2 3 correspondence should be sent to - Plant …...2018/01/30 · 126 Associated with ribosomal export complex1 (Arx1) and ARX1 little brother1 (Alb1) (Lo et al., 127 2010; Meyer

1

Running head: Ribosomal factors influence cold acclimation 1

2

correspondence should be sent to: 3

4

Joachim Kopka 5

address: Max-Planck-Institute of Molecular Plant Physiology, Department of Molecular 6

Physiology: Applied Metabolome Analysis, Am Mühlenberg 1, D-14476 7

Potsdam-Golm, Germany 8

phone: +49 (0) 331-567-8262 9

email: [email protected] 10

11

12

Plant Physiology Preview. Published on January 30, 2018, as DOI:10.1104/pp.17.01448

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon September 9, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

Plant temperature acclimation and growth rely on cytosolic ribosome 13

biogenesis factor homologs 14

15

Olga Beine-Golovchuk, Alexandre Augusto Pereira Firmino, Adrianna Dąbrowska, Stefanie 16

Schmidt, Alexander Erban, Dirk Walther, Ellen Zuther, Dirk K. Hincha, and Joachim Kopka 17

Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, D-14476 Potsdam-18

Golm, Germany 19

20

Corresponding author: Joachim Kopka ([email protected]) 21

22



3

Summary sentence 23

REI1-LIKE ribosome biogenesis factor homologs guide cold-acclimation and 60S subunit 24

accumulation for plant growth at alternating temperatures. 25

26

27

28

Author Contributions 29

J.K. and S.S. conceived the original research plans; O.B.G. with support of A.A.P.F. 30

performed the experiments, generated and characterized the mutant plants, established 31

experimental protocols and obtained experimental data; O.B.G., S.S., and A.D. performed 32

germination, growth and development analyses; E.Z. and D.K.H. supervised electrolyte 33

leakage assays; O.B.G., D.W., and J.K. performed transcriptome analyses; O.B.G., A.E., 34

and J.K. performed metabolome analyses; J.K. wrote the manuscript with support of O.B.G. 35

and contributions by all other authors. 36

37



4

Abstract 38

Arabidopsis (Arabidopsis thaliana) REI1-LIKE (REIL) proteins, REIL1 and REIL2, are 39

homologs of a yeast ribosome biogenesis factor (RBF) that participates in late cytoplasmic 40

60S ribosomal subunit maturation. Here, we report that the inhibited growth of the reil1-1 41

reil2-1 mutant at 10°C can be rescued by expression of N-terminal FLUORESCENT 42

PROTEIN (FP)-REIL fusions driven by the UBIQUITIN 10 promoter, allowing analysis of 43

REIL function in planta. Arabidopsis REIL1 appears to be functionally conserved, based on 44

the cytosolic localization of FP-REIL1 and the interaction of native REIL1 with the 60S 45

subunit in wild-type plants. In contrast to its yeast homologs, REIL1 was also present in 46

translating ribosome fractions. Systems analysis revealed that wild-type Arabidopsis 47

remodels the cytosolic translation machinery when grown at 10°C by accumulating cytosolic 48

ribosome subunits and inducing the expression of cytosolic rRNA, ribosomal genes, RBFs, 49

and translation initiation or elongation factors. In the reil1-1 reil2-1 mutant, all processes 50

associated with inhibited growth were delayed, although the plants maintained cellular 51

integrity or acquired freezing tolerance. REIL proteins were also implicated in plant-specific 52

processes: non-acclimated reil1-1 reil2-1 exhibited cold-acclimation responses including 53

activation of the DREB/CBF regulon. In addition, acclimated reil1-1 reil2-1 plants failed to 54

activate FLOWERING LOCUS T expression in mature leaves. In the wild type, REIL function 55

may therefore contribute to temperature perception by suppressing premature cold 56

responses during growth at non-stressful temperatures. In conclusion, we suggest that 57

Arabidopsis REIL proteins influence cold-induced plant ribosome remodeling and enhance 58

accumulation of cytosolic ribosome subunits after cold-shift either by de novo synthesis or by 59

recycling them from the translating ribosome fraction. 60

61



5

Introduction 62

In plants, cytosolic ribosomes are composed of the canonical eukaryotic small ribosomal 63

subunit (40S SSU), which involves the 18S ribosomal (r)RNA and approximately 32 64

ribosomal proteins (RPs). Cytosolic ribosomes also include the large ribosomal subunit (60S 65

LSU) that involves the 28S, 5.8S, and 5S rRNAs and approximately 48 RPs (Barakat et al., 66

2001). Cytosolic RPs are highly conserved across the eukaryotic kingdoms but plants have 67

between 2 and 7 paralogs of each RP (Barakat et al., 2001). Accordingly, the Arabidopsis 68

(Arabidopsis thaliana) genome contains ~221 genes that code for cytosolic RPs in addition 69

to 71 mitochondrial and 77 plastid RP genes (Sormani et al. 2011). These multiple plant 70

paralogs of each cytosolic RP family create the potential for highly diverse cytosolic 71

ribosome species that may function redundantly (Creff et al., 2010). However, the paralogs 72

of cytosolic RPs can differentially change phosphorylation status or abundance upon 73

environmental or nutritional cues (Chang et al., 2005; Wang et al., 2013; Browning and 74

Bailey-Serres, 2015) and apparently have specific developmental roles (Degenhardt and 75

Bonham-Smith, 2008; Byrne 2009; Horiguchi et al. 2012; Rosado et al., 2012). 76

The complex biogenesis of the 40S SSU and 60S LSU is initiated in the nucleolus, continues 77

in the nucleoplasm, and is completed after export to the cytosol by late maturation and 78

structural proof-reading steps that render the subunits translationally competent. Similar to 79

other eukaryotic organisms, a 43S preinitiation complex is formed prior to translation that 80

contains the eukaryotic initiation factors (eIFs). Under the guidance of eIF3, the preinitiation 81

complex recruits either the conserved eIF4F-complex or a plant specific eIFiso4F-complex. 82

These are circularized complexes composed of cap-bound messenger RNA (mRNA), eIF4 83

or eIFiso4, and poly(A)-binding protein (PAB). The combination of 43S and eIF4F-/eIFiso4F-84

complexes forms the start codon (AUG) scanning 48S complexes. AUG recognition triggers 85

60S LSU recruitment, the exit of eIFs 1, 2, 3, 5, and 6, and ultimately formation of the mRNA 86

decoding 80S monosomes or polysomes (Browning and Bailey-Serres, 2015). 87

While cytoplasmic mRNA translation is well investigated (Browning and Bailey-Serres, 88

2015), functional analysis of plant ribosome biogenesis is lacking. Due to the many 60S and 89

40S maturation steps, a multitude of eukaryotic ribosome biogenesis factors (RBFs) function 90

in the nucleolus, in the nucleoplasm or in the cytosol (Pendle et al., 2005; Palm et al., 2016). 91

Only 25% of the plant homologs of yeast (Saccharomyces cerevisiae) RBFs, the currently 92

best understood model organism, have been characterized so far (Weis et al., 2015). 93

Currently, the sparse knowledge of plant ribosome biogenesis and the investigated details of 94

pre-ribosomal (r)RNA processing indicate the existence of plant specific ribosome 95



6

biogenesis mechanisms that may have evolved to adapt the non-homeostatic plant system 96

to environmental changes (Weis et al., 2015). 97

The Arabidopsis zinc finger proteins REI1-LIKE1 (REIL1) and REIL2 were named after their 98

yeast homologs Rei1 (Required for isotropic bud growth1) and its paralog Reh1 (Rei1 99

homologue1), and were recently recognized as late stage RBF homologs that likely 100

participate in the cytoplasmic steps of cytosolic ribosomal maturation (Schmidt et al., 2013; 101

Weis et al., 2015). REIL1 and REIL2 apparently share evolutionary conserved functions with 102

their yeast homologs, indicated by REIL1 and REIL2 transcript co-expression and protein-103

protein interaction studies and through partial complementation of the yeast ∆rei1 mutant by 104

heterologous expression of REIL1 (Schmidt et al., 2013; Schmidt et al., 2014). Furthermore, 105

the loss of one or both paralogs showed that they were non-essential at standard growth 106

temperature but caused severe growth defects at suboptimal low temperature, namely 10°C 107

for Arabidopsis. These defects were surprisingly similar comparing the Arabidopsis mutants 108

(Schmidt et al., 2013) to the respective homologous yeast mutants (Iwase and Toh-e, 2004; 109

Lebreton et al., 2006; Parnell and Bass, 2009). 110

So far, the function of yeast Rei1 is the best characterized among the currently known REIL-111

homologs that appear exclusive in eukaryotes (Schmidt et al., 2013). The cytosolic Rei1 112

protein was discovered through a mitotic proliferation defect of the ∆rei1 mutant (Iwase and 113

Toh-e, 2004). This aspect was not further investigated when Rei1 was recognized as a late 114

cytosolic RBF that associated with the non-translating 60S LSU fraction (Hung and Johnson, 115

2006; Lebreton et al., 2006; Meyer et al., 2007). The current mechanistic model of late 60S 116

biogenesis in yeast (Lo et al., 2010; Panse and Johnson, 2010; Greber et al., 2016; Ma et 117

al., 2017) indicates a central role of Rei1 for the release of 60S nuclear export factors and 118

triggering final maturation steps to full translation competence. In detail, prior to the Rei1 119

interaction, the 60S nuclear export factor Ribosomal-like protein24 (Rlp24) is replaced in the 120

cytosol by Ribosomal protein of the large subunit24A (Rpl24A) or the almost identical 121

Rpl24B paralog. Rpl24 proteins were suggested as binding partners of Rei1 that recruit Rei1 122

to the 60S LSU (Lebreton et al., 2006; Lo et al., 2010). Bound Rei1 co-operates with Type III 123

j-protein1 (Jjj1) (Demoinet et al., 2007; Meyer et al., 2007) to activate Hsp70-type ATPases, 124

Ssa1 or Ssa2, which in turn release an export factor complex that is composed of 125

Associated with ribosomal export complex1 (Arx1) and ARX1 little brother1 (Alb1) (Lo et al., 126

2010; Meyer et al., 2010). Arx1-Alb1 release is required to release the two final 60S RBFs. 127

These RBFs are (1) the Nonsense-mediated mRNA decay3 (Nmd3) protein with a likely 128

double function in 60S LSU structural proof reading and as a 60S LSU nuclear export factor 129

(Johnson et al., 2002; Lo et al., 2010) and (2) the eukaryotic Translation initiation factor6 130

(Tif6 or eIF6), an anti-association factor, which is located on the pre-60S LSU surface that 131



7

interacts with the 40S SSU when forming the 80S ribosome (Basu et al., 2001; Klinge et al., 132

2011). Only release of both final RBFs renders yeast 60S LSU translationally competent. 133

Recent cryo-EM structure analyses captured reconstituted and native yeast 60S-Arx1-Alb1-134

Rei1 complexes at near atomic resolution (Greber et al., 2012; Greber et al., 2016). In these 135

complexes the middle part of Rei1, amino acid residues 145-261 that contain two zinc 136

fingers, is positioned close to the polypeptide tunnel exit. The C-terminal 95 amino acids, 137

residues 299-393, of Rei1 are fully inserted into the tunnel and span the distance from tunnel 138

exit to the peptidyl transferase active site (Greber et al., 2016). Prior to Rei1, the polypeptide 139

tunnel is occupied by the ~75 C-terminal amino acids of the nuclear pre-60S assembly and 140

export factor Nucleolar G-protein1, i.e. Nog1 (Wu et al., 2016). In contrast to the well-141

structured Rei1 C-terminus, the Rei1 N-terminus, residues 1-144, that contain the first zinc 142

finger was not visualized and is apparently disordered in the captured complex. Jjj1 maps to 143

the vicinity of the polypeptide tunnel exit close to Arx1 (Greber et al., 2012) and the Arx1-144

Alb1 complex is located in contact with Rei1 at the polypeptide tunnel exit (Greber et al., 145

2016). C-terminal fusions with Green fluorescent protein (GFP) or the tandem affinity 146

purification (TAP) tag render Rei1 non-functional. C-terminal deletion studies demonstrated 147

the requirement of up to 61 C-terminal amino acids, residues 333-393, and the presence of 148

an Arx1 interacting helix of Rei1. These results suggest that Rei1 proof-reading may test 149

polypeptide tunnel integrity in the cytosol (Greber et al., 2016). Additional functions of yeast 150

Rei1 remain to be discovered, such as the role of the disordered Rei1 N-terminus (Greber et 151

al., 2016) or a possible moonlighting function of non-ribosome bound Rei1 that may be 152

indicated by the initially discovered mitotic defect of ∆rei1 (Iwase and Toh-e, 2004). The role 153

of the Rei1 paralog, Reh1, is apparently equivalent to Rei1. Reh1 stabilizes the 60S LSU in 154

the absence of Rei1 (Parnell and Bass, 2009) and forms a complex with the 60S LSU with 155

the Reh1 C-terminus inserted into the polypeptide tunnel (Ma et al., 2017). 156

In contrast to yeast, the functional analyses of the likely Arabidopsis RBFs, REIL1 and 157

REIL2, are in their initial stages. Our previous reports (Schmidt et al., 2013; Schmidt et al., 158

2014) supported the hypothesis of a partial conservation of Arabidopsis REIL function with 159

yeast Rei1 and Reh1, but several observations indicate that evolution of Arabidopsis REIL 160

proteins diverged from yeast. (1) Heterologous expression only of Arabidopsis REIL1 but not 161

of REIL2 complemented the temperature dependent growth defect of the yeast ∆rei1 mutant 162

(Schmidt et al., 2013). (2) Different gene duplication events apparently created the two 163

paralogs in yeast and Arabidopsis independently (Schmidt et al., 2013), and (3) in contrast to 164

the four zinc finger domains present in Arabidopsis REIL1 and REIL2 that are arranged in 165

two C2H2 zinc finger pairs, namely ZF1/ZF2 at the N-terminus and ZF3/ZF4 in the middle of 166



8

the protein (Schmidt et al., 2013), the yeast paralogs contain only three zinc fingers (Iwase 167

and Toh-e, 2004; Greber et al., 2012). 168

To take the next step towards functional analysis of Arabidopsis REIL proteins we 169

investigated both, evidence of functional conservation and indications of plant specific 170

functions of the Arabidopsis REIL proteins, which may have been added on the evolutionary 171

path towards the multicellular embryophyte Arabidopsis. For this purpose, we first 172

established the previously created double mutant reil1-1 reil2-1 (Schmidt et al., 2013) as a 173

valid plant system for the investigation of REIL function in Arabidopsis. We characterized the 174

reil1-1 reil2-1 acclimation process to low temperature (10°C) in comparison to the 175

Arabidopsis Col-0 wildtype (WT) and found that this process likely involves ribosomal 176

biogenesis and/or ribosome subunit recycling, processes that we can currently not 177

distinguish with our methods. We demonstrated functional complementation of the growth 178

defect of reil1-1 reil2-1 in the cold and cytosolic protein localisation by re-introducing N-179

terminal Fluorescent protein (FP)-REIL fusion proteins. Furthermore, we demonstrated 180

association of REIL with cytosolic WT ribosomes and an enhancer role of REILs for 60S 181

subunit accumulation during cold-acclimation. Integrative metabolomic and transcriptomic 182

systems analyses of reil1-1 reil2-1 linked REIL proteins to higher level plant functions, such 183

as temperature perception. This association was indicated by premature triggering of cold-184

acclimation responses in reil1-1 reil2-1. Transcriptional compensation reactions in reil1-1 185

reil2-1 pointed towards a role of Arabidopsis REIL proteins for plant development at low 186

temperature that may reach beyond ribosomal 60S LSU biogenesis. 187

188



9

Results 189

The reil1-1 reil2-1 mutant stops growth and development when exposed to low 190

temperature. 191

At temperature conditions that were approximated to standard Arabidopsis laboratory 192

cultivations, namely 20-21°C with ~150 µmol m–2 s–1 photons during the day and 17-18°C 193

during the night (in the following referred to as “standard” conditions), reil1-1 reil2-1 194

germinated, grew, and developed almost indistinguishably compared to Col-0 (Figure 1). 195

Mutant plants at the ten-leaf stage, i.e. stage ~1.10 (Boyes et al., 2001), were slightly but not 196

significantly smaller than Col-0 (Figure 2 A-B). We confirmed the previous observation 197

(Figure 1A) that the young developing rosette leaves had a mild pointed leaves phenotype 198

(Schmidt et al., 2013). This leaf phenotype is a characteristic of many cytosolic ribosomal 199

mutants (Van Lijsebettens et al., 1994; Horiguchi et al., 2011). 200

At constant 10°C temperature (in the following called “low”), the mutant germinated and 201

reached the cotyledon stage but stopped to produce regular rosette leaves (Schmidt et al., 202

2013). Populations of reil1-1 reil2-1, nevertheless, survived at least 13 weeks of cultivation 203

on soil with temperatures set to 10°C during the day and 8°C at night (Figure 1B). The 204

mutation was apparently not lethal but caused a cold-conditional and extremely dwarfed 205

phenotype with few stunted leaves. The cold-arrested mutant was rescued by shift from low 206

to standard temperature (Figure 1E) but in contrast to the de-acclimating WT, reil1-1 reil2-1 207

entered a rapid flowering program. 208

The temperature dependent growth arrest that we first observed directly after germination in 209

the cold also occurred at the vegetative developmental stage ~1.10 (Boyes et al., 2001) after 210

shift from standard to suboptimal cultivation temperatures, namely to both, 10°C/8°C or 211

4°C/4°C during day and night, respectively (Figure 1C-D). The mutant and Col-0 WT 212

stopped rosette expansion growth and production of new leaves immediately after shift to 213

10°C or 4°C (Figure 2A-B) but only Col-0 resumed both processes after a lag-phase of 214

approximately 1 or 2 weeks, respectively. In contrast, reil1-1 reil2-1 maintained only minimal 215

extension growth and produced only few leaves even 13 weeks after shift to 10°C. Residual 216

extension growth and leaf formation of the mutant stopped completely at 4°C. The mutant 217

but not Col-0 accumulated intense purple violet pigmentation that is caused by activation of 218

Arabidopsis flavonol and anthocyanin metabolism (Schulz et al., 2015). Because changes of 219

flavonol and anthocyanin pool sizes in some flavonol biosynthesis pathway mutants cause 220

significant differences in freezing tolerance (Schulz et al., 2016), we applied an electrolyte 221

leakage based freezing tolerance assay (Rohde et al., 2014; Thalhammer et al., 2014) to 222



10

assess maintenance of reil1-1 reil2-1 cellular integrity in non-acclimated and cold acclimating 223

mature rosette leaves (Figure 2C). Reil1-1 reil2-1 did not differ from Col-0 in the non-224

acclimated state and furthermore did not lose cellular integrity even after weeks of growth 225

arrest at 10°C or 4°C (Figure 2C). Small differences of the mutant compared to WT indicated 226

a marginally faster acquisition of freezing tolerance (Figure 2C). 227

228

N-terminal Fluorescent Protein (FP) fusions of REIL1 and REIL2 localize to the cytosol 229

and restore reil1-1 reil2-1 growth at low temperature 230

To demonstrate complementation of the temperature dependent reil1-1 reil2-1 phenotypes, 231

we introduced N-terminal fusion proteins of REIL1 and REIL2 with the green fluorescent 232

protein (GFP) or the red fluorescent protein (RFP) into the mutant under control of the 233

constitutive UBIQUITIN 10 (UBQ10, AT4G05320) promoter (Supplemental Figure S1). 234

Attempts to introduce analogous C-terminal fusion proteins failed in agreement with the 235

known requirement of an unaltered and intact C-terminus for yeast Rei1 function (Greber et 236

al., 2016). 237



11

Introduction of FP-REIL2 reporter proteins into the reil1-1 reil2-1 mutant restored the 238



12

expected phenotype of the reil1-1 mutant that is highly similar to Col-0 WT (Schmidt et al., 239



13

2013). Two independently generated reporter lines UBQ10::GFP-REIL2 (line 41) and 240

UBQ10::RFP-REIL2 (line 109) that carried either of these expression cassettes in the reil1-1 241

reil2-1 mutant background and line UBQ10::REIL2 (line 95) that expressed REIL2 without 242

reporter gene fusion in reil1-1 reil2-1 exemplify our observations (Figure 3). In a previously 243

established in vitro germination assay (Schmidt et al., 2013) UBQ10::GFP-REIL2 (41) and 244

UBQ10::RFP-REIL2 (109) germinated at constant 10°C and generated first rosette leaves. 245

Germination kinetics were similar to the reil1-1 mutant that was slightly delayed compared to 246

Col-0 (Figure 3A,C). Line UBQ10::REIL2 (95) without a FP fusion was also indistinguishable 247

from reil1-1 (Figure 3C). After transfer to soil and continued cultivation at 10°C/8°C 248

(day/night) both, UBQ10::GFP-REIL2 (41) and UBQ10::RFP-REIL2 (109) developed 249

rosettes that were similar to reil1-1 and WT (Figure 3B). Line UBQ10::GFP-REIL2 (41) had a 250

mild pointed leaves phenotype in the cold (Figure 3B, sub-panel b). Timing of reil1-1 reil2-1 251

and Col-0 germination in vitro at 20°C was indistinguishable and approximately twice as fast 252

as at 10°C (Supplemental Figure S2). The presence of expression cassettes UBQ10::GFP-253

REIL2, UBQ10::RFP-REIL2, and UBQ10::REIL2 in the reil1-1 reil2-1 mutant background did 254

not affect timing of germination at 20°C. 255

Introduction of FP-REIL1 reporter proteins into the reil1-1 reil2-1 mutant restored the reil2-1 256

mutant phenotype. This phenotype is highly similar to the allelic reil2-2 mutant phenotype 257

and is characterized by delayed appearance of first rosette leaves at 10°C and spoon-258

shaped leaves (Schmidt et al., 2013). The reporter lines UBQ10::GFP-REIL1 (line 34) and 259

UBQ10::RFP-REIL1 (line 49) that carried the UBQ10::GFP-REIL1 and UBQ10::RFP-REIL1 260

expression cassettes in the reil1-1 reil2-1 mutant background germinated with the expected 261

delay compared to Col-0 (Figure 3A,D) and, as was expected, developed spoon-shaped 262

leaves after continued cultivation on soil at 10°C/8°C (day/night) (Figure 3B). The timing of in 263

vitro germination at 20°C was slightly delayed by the presence of the expression cassettes 264

UBQ10::GFP-REIL1, and UBQ10::RFP-REIL1 in the reil1-1 reil2-1 mutant background 265

(Supplemental Figure S2). 266

For localization studies, we selected lines UBQ10::RFP-REIL1 (49) and UBQ10::RFP-REIL2 267

(109) that expressed stable RFP-REIL reporter proteins in the reil1-1 reil2-1 mutant 268

background (Supplemental Figure S1C). In contrast, preparations of GFP-REIL reporter 269

proteins contained varying amounts of cleaved GFP that could not be completely 270

suppressed by protease inhibitor mixtures (data not shown). RFP-REIL1 was located in the 271

cytosol at 20°C and at 10°C (Figure 4A-C). The fluorescence signal was homogenous in the 272

cytosol and excluded from vacuoles, nuclei and the chloroplasts. RFP-REIL2 also located to 273

the cytosol both at 20°C and at 10°C (Figure 4D-F). In addition, the fluorescence signal was 274



14

also present in the nuclei of guard cells (Figure 4D) and at 10°C also in the nuclei of cells of 275



15

the root tip (Figure 4F). 276

The reil1-1 reil2-1 mutation delays accumulation of the 60S ribosomal subunit and of 277

cytosolic rRNA after 10°C cold shift 278

The preceding morphometric and complementation studies established the reil1-1 reil2-1 279

mutant as a viable system for the study of Arabidopsis REIL protein function. Furthermore, 280

we demonstrated that a shift to 10°C was sufficient to turn off extension growth of pre-281

existing mature leaves and the development of new leaves in the reil1-1 reil2-1 mutant 282

without apparent effects on cell integrity of mature leaf tissue (Figure 2). Based on these 283

observations, we performed an integrated system analysis of reil1-1 reil2-1 mutant and 284

investigated in detail the differential response of mutant and Col-0 WT before and after cold 285

shift. Throughout the following studies, we applied the 20°C to 10°C cold acclimation 286

experimental design C (Figure 1C) and focused our experiments on mature leaf tissue. This 287

choice facilitated combined differential analyses of relative transcript and metabolite levels 288

and importantly, provided sufficient leaf material for ribosome analyses. 289

Two other phenotypic hallmarks of Rei1p deficiency are known in yeast besides cold 290

sensitivity of growth. The deletion of yeast Rei1p causes a reduction of the relative amount 291

of the cytosolic 60S LSU under cold-conditions (Hung and Johnson, 2006). In addition, so-292

called polysome half-mers appear in the cold, i.e. mRNAs with one or more 80S ribosomes 293

and an additional 40S subunit attached (Parnell and Bass, 2009; Greber et al., 2016). To 294

investigate these phenotypes, we started our system analysis with a comparison of reil1-1 295

reil2-1 and Col-0 ribosome composition. 296

Microfluidic electrophoresis of total RNA preparations from mature leaf tissue enabled 297

relative quantitation of cytosolic and chloroplast ribosomal RNAs (rRNAs), specifically 298

cytosolic 18S and 25S rRNAs compared to plastid 16S and 23S rRNAs (Supplemental 299

Figure S3). 5S and 5.8S rRNAs were detectable but not clearly separated. We analyzed 23S 300

rRNA by summation of the two previously described post-maturation fragments 23S´ and 301

23S´´ that result from hidden breaks of the mature 23S rRNA (Nishimura et al., 2010; Tiller 302

et al., 2012) Fragments 23S´ and 23S´´ were abundant in all analyzed samples. A third small 303

23S´´´ hidden break product and the potential full size rRNA precursor (Tiller et al., 2012) 304

were detectable only at very low intensity and disregarded in this study. 305

Ratios of cytosolic compared to chloroplast rRNAs changed during Col-0 cold acclimation 306

(Figure 5A-C) after shift to the 10°C cultivation regime (Figure 1C). The 25S/23S rRNA and 307

the 18S/16S rRNA ratios both increased one week after cold shift (Figure 5A-B). This 308



16

observation indicated enhanced de novo synthesis of cytosolic rRNA relative to chloroplast 309

rRNA. The ratio of the cytosolic large subunit 25S compared to the cytosolic small subunit 310

18S rRNA remained unchanged (Figure 5C). The accumulation of cytosolic rRNA relative to 311

chloroplast rRNA preceded the resumption of growth and development of Col-0 (Figure 2A-312

B). We concluded that cold acclimation causes an altered balance between cytosolic and 313

chloroplast ribosome biogenesis and therefore represents a condition that is suitable for the 314

analysis of potential cytosolic ribosome biogenesis factors, such as the Arabidopsis REIL 315

proteins (Schmidt et al., 2013, Weis et al., 2015). Cytosolic rRNA accumulation in the reil1-1 316

reil2-1 mutant after exposure to cold was not fully abolished but delayed compared to cold 317

acclimating Col-0 (Figure 5A-B). We therefore hypothesized that REIL proteins have a role in 318

enhancing the kinetics of cytosolic ribosome biogenesis in the cold. 319

To further validate this hypothesis, we analyzed the ribosome composition of mutant and 320

Col-0 leaves by differential ultracentrifugation (Figure 5D-F). Conventional ultracentrifugation 321

methods of plant ribosome/polysome preparation, e.g. (Mustroph et al., 2009), were initially 322

adapted from technologies developed for organisms, such as yeast, that contain only small 323

and negligible amounts of prokaryotic-type mitochondrial ribosomes (Parnell and Bass, 324

2009; Greber et al., 2016). Plant leaves, however, contain large amounts of chloroplast 325

ribosomes that cannot be neglected (Tiller et al., 2012). The chloroplast ribosomes were not 326



17

separated from cytosolic ribosomes by current methods (Mustroph et al., 2009). For our 327

study, we developed a differential ultracentrifugation protocol with a sedimentation gradient 328

that was optimized for the separation of the cytosolic 60S and the chloroplast 50S large 329

subunits (Supplemental Figure S3). The modified sedimentation gradient included the 30S 330

and 40S small subunits, the 50S and 60S large subunits, 70S and 80S monosomes, and in 331

addition, a mixed chloroplast and cytosolic polysome fraction (Supplemental Figure S3A-B). 332

Detailed microfluidic electrophoretic analysis of RNA preparations from respective fractions 333

of the sedimentation gradient revealed that the cytosolic 60S fraction separated from the 334

chloroplast 50S fraction and from the 80S monosomes (Supplemental Figure S3C-D). The 335

70S monosomes were present at low abundance between the 60S and 80S fractions. The 336

30S and 40S subunit fractions were clearly separated from the 50S subunits but overlapped 337

and formed a 30S-enriched fraction followed by a 40S-enriched fraction. Cytoplasmic and 338

chloroplast polysome fractions also overlapped and did not allow unambiguous diagnosis of 339

the presence of cold-induced cytosolic polysome half-mers (Parnell and Bass, 2009; Greber 340

et al., 2016). 341

In the non-acclimated state, reil1-1 reil2-1 ribosome preparations were indistinguishable from 342

Col-0 (Figure 5D). One day after cold shift cytosolic and chloroplast ribosome subunits 343

increased relative to the strongly reduced polysome fractions. Both the mutant and Col-0 344

had increased amounts of ribosome subunits after cold shift, but reil1-1 reil2-1 clearly 345

accumulated fewer ribosome subunits than Col-0. One week after cold shift Col-0 increased 346

the 60S fraction relative to the 50S fraction, whereas reil1-1 reil2-1 lagged behind and still 347

had significantly reduced amounts of 60S LSUs. This observation was confirmed by 348

analyses of relative peak abundances of the ribosome fractions after blank gradient 349

subtraction of absorbance (A254nm) and normalization to total absorbance of all observed 350

ribosome fractions (Figure 5E). A ratio-metric analysis of normalized 60S to 50S abundance 351

(Figure 5F) corresponded to our 25S/23S rRNA ratio data (Figure 5A). In Col-0 the amount 352

of the 60S subunit fraction increased relative to the 50S subunits during cold acclimation. In 353

contrast, the accumulation of 60S subunits was significantly delayed in the mutant. 354

The REIL1 protein is associated with 60S, 80S and polysome fractions 355

Peptide antibodies, anti-atREIL1.1 and anti-atREIL2.1, were directed against variable 356

regions at the C-terminus of REIL1 and REIL2. These peptides detected the proteins, REIL1, 357

45,998 Da with 404 amino acids, and REIL2, 44,987 Da with 395 amino acids, e.g. 358

(https://apps.araport.org/thalemine/begin.do), in total protein preparations of 20°C/18°C 359

(day/night) cultivated Col-0 at an electrophoretic mobility of approximately 35 kDa. The 360

proteins were not detectable in 20°C/18°C (day/night) cultivated reil1-1 reil2-1 (Supplemental 361



18

Figure S1). Western blots of Col-0 ribosome fractions from the modified sucrose density 362

ultracentrifugation gradients using anti-atREIL1.1 and anti-atREIL2.1 revealed the presence 363

of REIL1 in the non-translating 60S fraction but also in the 80S and polysome fractions 364

(Figure 6). The anti-atREIL1.1 antibody detected only very weak signals of the 35kDa 365

protein. Instead, up to three cleavage products of REIL1 were present after preparation of 366

the ribosome proteins from the ultracentrifugation fractions. These fragments were present 367

at low abundance in total protein preparations of the reil2-1 mutant (Figure 6; Supplemental 368

Figure S1). The anti-atREIL2.1 Western analysis showed very weak signals of a 35 kDa 369

protein and did not reveal REIL cleavage products (data not shown). 370

Metabolic systems analysis of reil1-1 reil2-1 reveals a metabolic phenotype in the non-371

acclimated state and deviations from Col-0 after long-term acclimation to 10°C 372

To gain further insights into the consequences of the reil1-1 reil2-1 mutation and the 373

absence of REIL proteins from the Arabidopsis system, we profiled the metabolome changes 374

of the non-acclimated and the cold acclimating mutant with high temporal resolution in the 375

first day after cold shift and at longer intervals during the following 4 weeks in the cold 376

(Supplemental Table S1). Phenotyping of the primary metabolome revealed 50 relevant 377



19

either genotype-differential or cold responsive metabolites (Figure 7A) that were retrieved 378

from the non-targeted profiles by analysis of variance (ANOVA). Eighteen of these 379

metabolites were 10°C shift responsive in Col-0 (Supplemental Table S1). Sixteen of these 380

metabolites were previously reported to also increase following a 4°C cold shock (Kaplan et 381

al., 2004; Kaplan et al., 2007; Guy et al., 2008). Only myo-inositol, which decreased after 382

cold shock in the previous 4°C analyses, increased significantly in our current 10°C shift 383

experiments (Supplemental Table S1). 384

The responses of the reil1-1 reil2-1 mutant and Col-0 to the 10°C shift were highly similar up 385

to two days after cold shift (Figure 7). However, the non-acclimated reil1-1 reil2-1 mutant 386

already had a hidden metabolic phenotype compared to non-acclimated Col-0 (Figure 7B, 387

arrow). Many of the changed metabolite levels in the non-acclimated mutant were similar to 388

the levels observed in cold acclimating Col-0 (Figure 7A). This observation included the well-389

characterized environmental stress metabolites of Arabidopsis, such as proline and raffinose 390

(Figure 7C), but also other carbohydrates and amino acids that typically accumulate upon 391

cold shock (Guy et al., 2008). Two days after cold shift, mutant metabolism began to differ 392

significantly from Col-0. Rather than deviating from the general trend of accumulating 393



20

carbohydrates and amino acids, most cold responsive metabolites accumulated further and 394

beyond Col-0 levels in the mutant (Figure 7A-B; Supplemental Table S1). No metabolite pool 395

had constitutively lower levels in the mutant, whereas phosphate, β-alanine, proline, 396

galactinol and raffinose remained upregulated throughout the complete time course (Figure 397

7C; Supplemental Table S1). 398

To further characterize the metabolic phenotype of reil1-1 reil2-1 at standard cultivation 399

temperature, we compared the non-acclimated mutant to the time course of cold acclimating 400

Col-0 (Supplemental Figure S4). Metabolic profiles of non-acclimated reil1-1 reil2-1 were 401

similar to Col-0 specifically the first two days after cold shift. This similarity was revealed by 402

both hierarchical clustering and principal component analyses (Supplemental Figure S4A). 403

Furthermore, the relative levels of metabolites in the non-acclimated reil1-1 reil2-1 highly 404

correlated with the respective levels of Col-0 during the first two days after cold shift and 405

maintained correlation beyond these time points (Supplemental Figure S4B). We 406

hypothesized that the non-acclimated mutant may be temperature sensitized and was 407

triggering premature metabolic cold responses at standard cultivation temperature. 408

Previous studies indicated that many cold responsive primary metabolite pools were not 409

highly cold specific but may also be modulated by heat or other stresses (Kaplan et al., 410

2004; Kaplan et al., 2007; Supplemental Table S1). Therefore, our temperature sensitization 411

hypothesis required additional validation by transcriptome profiling. 412

Reil1-1 reil2-1 activates transcriptional cold acclimation responses at standard 413

temperature 414

To validate our previous observations and to extend our insight into global systems 415

responses of the mutant, we performed transcriptome profiles of mature leaves from mutant 416

and Col-0 WT at informative time points, i.e. the non-acclimated state (0 days of acclimation, 417

0 day), and after 1 day, 1 week and 3 weeks of 10°C cold acclimation (Supplemental Table 418

S2). These time points were selected according to the preceding growth analyses (Figure 2) 419

and the better time-resolved metabolome analyses (Figure 7, Supplemental Figure S4). In 420

the non-acclimated state, we aimed to further reveal the details of a hidden mutant 421

phenotype. At 1 day and 1 week we analyzed the short-term and long-term differential 422

responses of the mutant that are not yet associated with differential growth. At 3 weeks after 423

cold shift we investigated the long-term acclimation defect of the mutant, namely the effects 424

that were associated with the inability of the mutant to resume growth. 425



21

The non-acclimated reil1-1 reil2-1 mutant differentially expressed 428 genes compared to 426

non-acclimated Col-0 (Supplemental Table S3). These differentially expressed genes 427

(DEGs) encoded 287 transcripts with increased abundance and 141 with decreased 428

abundance (Table 1). 42.2 % (121) and 20.6 % (29). In sum, 150 of these transcripts (Table 429

1) were shared with the respectively changed 10°C cold responsive transcripts of Col-0 at 1 430

d, 1 w, or 3 w after shift, which were also calculated relative to the non-acclimated Co-0 WT. 431

Thirty one of the 150 shared differentially expressed genes had constitutively increased 432

transcript abundance in Col-0 even throughout the complete cold acclimation time course 433

(Table 1, Supplemental Table S3). In addition, relative expression levels of these shared 150 434

DEGs were highly correlated between the non-acclimated mutant and the respective 435

transcript levels in Col-0 1 d, 1 w or 3 w after acclimation to 10°C (Supplemental Figure S5). 436

However, the shared DEGs represented only a small fraction of the 10°C responsive genes 437

of Col-0 WT (Table 1). 438

For this reason, we used functional enrichment analysis of differential gene expression by 439

parametric analysis of gene set enrichment (PAGE, Du et al., 2010) to test the full non-440

filtered differential gene expression data set of non-acclimated reil1-1 reil2-1 relative to non-441

acclimated Col-0 WT. The method assessed enrichment of up- or down regulation among 442

the gene sets of 1940 gene ontology (GO) terms. These GO terms contained 135 that were 443

linked to acclimation or responses to stimuli and stresses (Figure 8A, Supplemental Table 444

S4). Next to the differential gene expression enrichment analysis of non-acclimated reil1-1 445

reil2-1, we performed in parallel equivalent PAGE enrichment analyses of the full non-filtered 446

differential gene expression data sets of 1 d, 1 w or 3 w cold-acclimating Col-0, which were 447

also calculated relative to non-acclimated Col-0. These analyses allowed comparison of the 448

mean log2-fold expression changes (FCs) of the gene sets defined by the GO terms between 449

the non-acclimated mutant and the three time points of 10°C acclimating Col-0 WT. 450

Pearson´s correlation analysis of the mean log2-FCs across the 135 stress related GO terms 451

revealed linear correlation between the mean log2-FCs of non-acclimated reil1-1 reil2-1 and 452

Col-0 at 1 d after shift to 10°C. The correlation attenuated over time but mean log2-FC of one 453

GO term remained highly associated (Figure 8B). To identify this and other GO terms that 454

were relevant for insights into the physiological state of the non-acclimated mutant, we 455

limited the analysis to GO terms with mean log2-FC > +0.1 or < -0.1. Furthermore, we ranked 456

the resulting 59 from the initial 135 GO terms according to their significance of enrichment 457

using z-scores (Du et al., 2010) and considered the GO terms with the top10 z-score values 458

to be most informative. All calculated mean log2-FC, z-scores and respective P-values are 459

reported within the supplement data (Supplemental Table S4). 460



22

The term with highest mean log2-FC was GO:0009631 “cold acclimation” and identical with 461

the persistently correlated term of our correlation analysis (Figure 8B). This GO term was 462

followed by GO:0010286 “heat acclimation” and two terms, GO:0009414 and GO:0009415, 463

with highly overlapping gene sets that represented responses to water limitation (Figure 8A). 464

The triggering of temperature acclimation responses in the non-acclimated mutant was 465

highly specific, because GOs that represented the general responses to temperature shifts, 466

stresses, or stimuli were not prematurely activated. In the case of GO:0033554 “cellular 467

response to stress” the mean log2-FC was even significantly lower in the non-acclimated 468

mutant relative to WT (Figure 8A). All the mentioned general GO terms, including 469



23

GO:0010286 “heat acclimation” and to a minor extend also GO: 0009408 “response to heat” 470

were part of the Col-0 WT response to the 10°C cold shift. Enrichment of drought, salt, 471

osmotic stress, and abscisic acid related GO terms were also part of the Col-0 10°C 472

response, but mean log2-FC did not exceed +0.1 in non-acclimated reil1-1 reil2-1 (Figure 473

8A). The terms with the most decreased transcript abundance, which were shared between 474

the non-acclimated mutant and 1 day cold acclimating Col-0, were GO:0071446 “cellular 475

response to salicylic acid stimulus” and GO:0031669 “cellular response to nutrient levels”. 476

The decreased responses to light or radiation and to brassinosteroid stimuli in the non-477

acclimated mutant were not part of the Col-0 cold response. 478

For further enrichment analysis we applied the same selection criteria, mean log2-FC > +0.1 479

or < -0.1 and selection of the most significant enrichments according to z-score values, to all 480

included 1940 GO terms (Supplemental Figure S6). The previously identified water limitation 481

GOs and in addition two flavonoid pathway related GO terms, GO:0009812 and GO:000983, 482

ranked highest among the GOs with increased transcript abundance. This observation was 483

again shared between non-acclimated mutant and acclimating Col-0. In contrast, the top 484

scoring down regulated terms were mostly specific to the non-acclimated mutant and related 485

to morphogenesis/development, the structural component of the chloroplast, nitrogen-486

compound metabolism, and the cell wall (Supplemental Figure S6). 487

We subsequently analyzed the set of genes that were both, changed in the non-acclimated 488

mutant (Supplemental Table S3) and annotated by the GO terms, GO:0009631 “cold 489

acclimation” or GO:0009409 “response to cold”. We found 8 DEGs that belonged to these 490

GO terms. The well-known regulators of cold acclimation (Thomashow 1999; Shinozaki et 491

al., 2003), C-REPEAT/DRE BINDING FACTOR1/DEHYDRATION-RESPONSIVE ELEMENT 492

BINDING PROTEIN1B (CBF1/DREB1B, AT4G25490.1), CBF2/DREB1C (AT4G25470.1), 493

and CBF3/DREB1A (AT4G25480.1) were part of this set (Figure 9A). Together with COLD-494

REGULATED15A (COR15A, AT2G42540.1), COR15B (AT2G42530.1) and COLD-495

INDUCED2 (KIN2, AT5G15970.1) (Figure 9B) the three regulators scored also high as 496

robust cold responsive genes compared to a previous meta-analysis of transcriptional 497

responses to 4°C cold stress (Hannah et al., 2005). 498

We extended the same intersection analysis to the heat GO terms and found only one 499

significant DEG in the non-acclimated mutant that belonged to GO:0010286 “heat 500

acclimation”, namely S-PHASE KINASE-ASSOCIATED PROTEIN2B (SKP2B, 501

AT1G77000.1). This protein is part of an E3-ubiquitin-ligase complex that degrades 502

ARABIDOPSIS THALIANA HOMOLOG OF E2F C (AtE2Fc, AT1G47870.1) a likely regulator 503



24

of cell division transition from skotomorphogenesis to photomorphogenesis (del Pozo et al., 504



25

2002). No significant DEG was found among the more general gene set of GO: 0009408 505

“response to heat”. The enrichment result of the heat related GO terms in non-acclimated 506

reil1-1 reil2-1 was explained by slight increases of mRNA abundance of many genes from 507

the GO term, but none of the genes was significantly changed in expression. We 508

subsequently investigated expression of genes that encode DREB2 proteins in more detail 509

(Figure 9C). DREB2 proteins are transcription factors that are part of the DREB/CBF-510

regulon and share the regulation of a subset of genes with DREB1/CBF factors (Yamaguchi-511

Shinozaki and Shinozaki, 2009; Lata and Prasad, 2011). Through this interaction, the 512

DREB/CBF-regulon integrates control of gene expression following drought and cold stress. 513

In contrast to DREB1/CBF gene expression that is rapidly activated upon cold stress, 514

expression of DREB2 genes is primarily activated upon heat and osmotic stresses. For this 515

reason, DREB2 genes are assigned to the heat, water limitation, and osmotic stress related 516

GO terms. mRNA levels of both DREB2A and DREB2B were only slightly increased in non-517

acclimated reil1-1 reil2-1 (Figure 9C), but increased significantly as part of the long-term (≥ 1 518

w) Col-0 response to 10°C (Figures 8-9). 519

Together with the activated expression of the DREB2A and DREB2B, gene expression of 520

the water limitation response terms, GO:0009414 and GO:0009415, was activated during 521

Col-0 acclimation to 10°C (Figure 8). Again, the enrichment result was based predominantly 522

on a small overall increase of expression of many genes. The gene sets of the water 523

limitation GO terms overlapped with the sets defined by heat-stress GOs, e.g. DREB2A and 524

DREAB2B (Figure 9C), but also with the cold stress GO terms (Figure 9A-B). In detail, 525

twenty eight of 183 cold response genes also belonged to the water limitation GOs, including 526

CBF1/DREB1B (AT4G25490.1), CBF3/DREB1A (AT4G25480.1) and KIN2 (AT5G15970.1). 527

Next to the overlapping genes, mRNAs of two water limitation specific genes were 528

significantly changed in the non-acclimated mutant, namely LIPID TRANSFER PROTEIN4 529

(LTP4, AT5G59310.1) and HISTONE1-3 (HIS1-3, AT2G18050.1). HIS1-3 encodes a drought 530

inducible linker histone that is preferentially expressed in younger leaf tissue and root tips 531

(Ascenzi and Gantt, 1999) and has a cell to cell mobile mRNA (Thieme et al., 2015). 532

Reil1-1 reil2-1 delays and subsequently hyper-activates cold triggered expression of 533

translation and ribosome related genes 534

Because the absence of REIL proteins delayed accumulation of the eukaryotic 60S 535

ribosomal subunit upon shift to low temperature, we searched for transcriptional responses 536

that were likely associated with this defect or that may partially compensate for REIL 537

deficiency. For this purpose, we focussed on ribosome and translation related genes, such 538

as the members of the global GO terms GO:000584 “ribosome” and GO:0006412 539



26

“translation” and included more specified GO terms of cellular components and biological 540

processes (Figure 10). Col-0 highly activated gene expression of cytosolic ribosome and 541

translation related genes relative to the non-acclimated state at 1 day after 10°C cold shift. 542

This activation subsequently attenuated. In contrast, reil1-1 reil2-1 delayed these responses, 543

as was revealed by enrichment analysis of differential gene expression in the mutant 544

compared to Col-0 at each time point (Figure 10A). As a result of the delay, ribosome and 545

translation related gene expression in reil1-1 reil2-1 was first reduced relative to Col-0 and 546

then increased both, at 1 and 3 weeks after shift to 10°C. This pattern of differential gene 547

expression was specific for the structural genes that constitute the cytosolic 60S and 40S 548



27

ribosomal subunits (Barakat et al., 2001; Chang et al., 2005; Giavalisco et al., 2005) and did 549

not extend to the structural genes of chloroplast ribosomes. These observations were 550

confirmed (Figure 10B) by additional analyses of the functional bins, that are equivalent to 551

GO terms but were defined by the MapMan and PageMan software developers (Thimm et 552

al., 2004; Usadel et al. 2006). Among the translation related GO terms, translation 553

elongation followed the general trend of structural cytosolic ribosome genes, whereas the 554

terms translation initiation and termination were activated in the mutant throughout 10°C cold 555

acclimation (Figure 10A). 556

For a detailed analysis of relevant DEGs we extracted 74 ribosome- or translation-related 557

genes that were significantly changed at one or more of the four analysed time points 558

(Supplemental Table S5). Thirty-six of these DEGs were structural constituents of the 559

cytosolic 60S and 40S subunits. Nine DEGs were part of translational initiation factors. One 560

DEG was a translational elongation factor. Five DEGs were aminoacyl-tRNA synthetases 561

and nine genes were ribosome biogenesis factors. Furthermore, five of the 74 DEGs were 562

previously annotated homologs of the yeast cytosolic 60S maturation machinery (Schmidt et 563

al., 2013), namely the RLP24-homolog (AT2G44860), the RPL24A gene (AT2G36620), the 564

RPP0A (AT2G40010), the TIF6-homolog (AT3G55620), and a SSA1|2-homolog 565

(AT3G09440.1). In addition, three previously studied plant biogenesis factors were present 566

in this gene set, namely ESSENTIAL NUCLEAR PROTEIN 1 (ENP1, AT1G31660.1), 567

HOMOLOGUE OF YEAST BRX1-1 (BRX1-1, AT3G15460.1) and NUCLEOLIN 2 (NUC2, 568

AT3G18610.1) (Weis et al., 2015). 569

With few exceptions, such as RPL3B (AT1G61580) or the RPL13 homolog (AT3G48130), 570

the differential gene expression pattern of the 74 extracted DEGs matched to the general 571

expression trend of their respective functional classes (Supplemental Table S5). One to 572

three weeks after shift to 10°C most genes had increased mRNA abundance relative to Col-573

0, as exemplified by the 60S constituents RPP0A (AT2G40010) or RPL24A (AT2G36620) 574

and the 40S constituent RPS8B (AT5G59240). Surprisingly, twelve DEGs belonged to the 575

plastid 50S and two to the 30S ribosomal subunit. In contrast to the cytosolic RPs, the 576

chloroplast RP components were down regulated (Supplemental Table S5), e.g. the 50S 577

component PRPL11 (AT1G32990) or the 30S component PRPS17 (AT1G79850). 578

Some ribosome and translation related genes deviated from the two general patterns of the 579

up regulated cytosolic and down regulated chloroplast RPs. The deviating genes had mostly 580

constitutively increased mRNA levels in the mutant relative to Col-0, for example, the 581

POLY(A)-BINDING PROTEIN (PAB5, AT1G71770) or the EUKARYOTIC TRANSLATION 582



28

INITIATION FACTOR 3 SUBUNIT C2 (EIF3C2, AT3G22860) of Arabidopsis eukaryotic 583

translation initiation factor 3 (EIF3). The constitutive up regulation of EIF3C2 mRNA relative 584

to WT (Supplemental Table S5) was an exception compared to the other differentially 585

expressed components of EIF3 (Burks et al., 2001). EIF3 subunit G2 (EIF3G2, AT5G06000) 586

had first lower then higher mRNA levels relative to Col-0 while EIF3 subunit H1 (EIF3H1, 587

AT1G10840) had decreased transcript levels. Similarly, cytosolic aminoacyl-tRNA 588

synthetase mRNAs (AT3G42723 and AT3G30770) were constitutively up regulated or 589

activated after cold shift, e.g. the cytosolic threonyl-tRNA synthetase (AT1G17960). 590

Reil1-1 reil2-1 does not activate FLOWERING LOCUS T in mature leaves after cold 591

shift 592

The transcripts of threonyl-tRNA synthetase (AT1G17960), aminoacyl-tRNA synthetase 593

(AT3G42723), and EIF3C2 were also among a set of 64 genes with a greater than 4-fold 594

change in expression in reil1-1 reil2-1 after 1 day, 1 week and 3 weeks at 10°C. Almost two-595

thirds (41) of these 64 transcripts were already significantly different from WT in the non-596

acclimated state and may represent candidates of genes with REIL dependent gene 597

expression control or constitutive compensation responses to REIL deficiency (Supplemental 598

Table S6). The 64 genes did not generate significant GO enrichment results when analysed 599

by singular enrichment analysis (Du et al., 2010), but FLOWERING LOCUS T (FT, 600

AT1G65480.1) and genes encoding MADS domain transcription factors were prominent 601

within this gene set (Figure 11). 602

In contrast to Col-0, FT expression was not activated in reil1-1 reil2-1 after cold shift (Figure 603

11). FT is the key mobile flowering signal, the “florigen” that is produced in leaves, the tissue 604

that we analyzed in this study, and acts at the shoot apex by triggering the transition from 605

vegetative to reproductive growth. mRNAs of down-stream elements of FT mediated flower 606

induction were detectable in mature leaves. In agreement with the lack of FT activation 607

SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1/AGL20, AT2G45660.1) and 608

AGAMOUS-LIKE 24 (AGL24, AT4G24540.1) were down regulated in reil1-1 reil2-1 leaves 609

(Figure 11). Transcripts of the FT partner protein FLOWERING LOCUS D (FD, 610

AT3G10390.1), however, remained unaffected as was expected of FD, which is mainly 611

expressed in the shoot apex (Kobayashi and Weigel, 2007). Transcripts of the FT/FD 612

activated meristem identity genes, LEAFY (LFY, AT5G61850.1) and APETALA1 (AP1/AGL7, 613

AT1G69120.1) were also detectable in our mRNA preparations from mature leaves but were 614

not differentially expressed. 615



29

To further dissect the lack of FT induction in reil1-1 reil2-1 we analyzed expression of 616



30

vernalization factors and of FLOWERING LOCUS C (FLC, AT5G10140.1). FLC is one of the 617

floral repressors that functions in leaves by repressing FT expression and in the shoot apical 618

meristem by repressing FD expression (Kobayashi and Weigel, 2007). FLC is a central 619

component of the vernalization response pathway and has decreased mRNAs levels in 620

vernalized leaves (Wellmer and Riechmann, 2010). Thus, vernalization releases FLC-621

mediated inhibition of FT expression in the leaf and FD in the shoot apical meristem as 622

prerequisites to the initiation of reproductive growth. If this pathway was responsible for the 623

lack of FT induction in reil1-1 reil2-1 leaves, vernalization responses would be absent in 624

reil1-1 reil2-1 and FLC expression would be up regulated. We found the opposite of our 625

expectations occurred. Vernalization responses were not prematurely activated in non-626

acclimated reil1-1 reil2-1 and like in Col-0, were strongly activated after 10°C cold shift 627

(Figure 11; Supplemental Table S6). For example, transcripts of the VERNALIZATION 628

INSENSITIVE3 (VIN3, AT5G57380.1), a cold specific component of the polycomb repressive 629

complex 2 (Lee et al., 2015), and VERNALIZATION INDEPENDENCE3 (VIP3, 630

AT4G29830.1) were increased in both the mutant and Col-0 (Figure 11). Apparently reil1-1 631

reil2-1 has no premature activation of vernalization and WT-like vernalization responses 632

(Song et al., 2012; Sun et al., 2013). Also contrary to our expectations, FLC expression 633

decreased much more in cold acclimating reil1-1 reil2-1 compared to Col-0 and surprisingly, 634

FLC expression was also much lower prior to vernalization in the non-acclimated mutant 635

(Figure 11). 636

Obviously the vernalization pathway did not explain the lack of FT activation in reil1-1 reil2-1. 637

As a consequence, we investigated alternative FT effectors in the leaf (Wellmer and 638

Riechmann, 2010). Neither the transcripts of the activator CONSTANS (CO, AT5G15840.1) 639

nor the mRNAs of the FT repressors TEMPRANILLO 1 (TEM1, AT1G25560.1), 640

TEMPRANILLO 2 (TEM2, AT1G68840.1) SHORT VEGETATIVE PHASE (SVP/AGL22, 641

AT2G22540.1), SCHLAFMUTZE (SMZ, AT3G54990.1), SCHNARCHZAPFEN (SNZ, 642

AT2G39250.1), TARGET OF EARLY ACTIVATION TAGGED 1-3 (TOE1-3, AT2G28550.1, 643

AT5G60120.1, AT5G67180.1) nor the splice variant 2 mRNA of FLOWERING LOCUS M 644

(FLM/AGL27, AT1G77080.2) that was part of our transcriptome analysis were differentially 645

expressed (Supplemental Table S6, Figure 11). 646

Among the remaining differentially expressed genes, other AGAMOUS-LIKE (AGL) 647

transcription factors are part of our set of 64 top DEG (Figure 11, Supplemental Table S6). 648

We found FLM-independent vernalization induced AGL19 (AT4G22950.1) (Schönrock et al., 649

2006; Liu et al., 2008) to have constitutively increased transcript levels in the mutant. Over-650

expression of AGL19 activates FT in a FLC-independent manner (Kim et al., 2013; Kang et 651



31

al., 2015). We therefore concluded that the block of FT activation in reil1-1 reil2-1 is both 652

downstream of AGL19 mediated FT activation and downstream of FLC mediated release of 653

FT repression. 654

In addition, eponymous AGAMOUS (AG, AT4G18960.1; Figure 11) and AGL42 (also named 655

FOREVER YOUNG FLOWER, AT5G62165.1; Supplemental Table S6) had constitutively 656

decreased mRNA levels in reil1-1 reil2-1 leaves. The relevance of these observations 657

remained unclear, because both genes are known for their roles in flower development 658

rather than for a function in leaf differentiation. AG is the shoot apex expressed floral organ 659

identity gene responsible for stamen- and carpel-formation. AG controls flower development 660

among other mechanisms by suppression of the leaf development program in emerging 661

floral primordia (Ó’Maoiléidigh et al., 2013). In agreement with reduced AG expression in 662

reil1-1 reil2-1 leaves, the transcript of CURLY LEAVES (CLF, AT2G23380.1) that 663

suppresses ectopic expression of AG in leaves (Kim et al., 1998) was not activated. AGL42 664

is highly expressed in young flowers prior to pollination rather than in leaves and controls 665

floral senescence and abscission (Chen et al., 2011). 666

667



32

Discussion 668

Cold acclimation of Col-0 WT is a relevant process for the investigation of cytosolic 669

RBFs 670

Our first aim was to establish an experimental setup that enables the study of conserved or 671

plant specific functions of Arabidopsis REIL proteins and of their proposed role in cytosolic 672

ribosome biogenesis (Schmidt et al., 2013; Schmidt et al., 2014). We previously discovered 673

that the cold impact on growth of the Arabidopsis single and double reil mutants and 674

respective mutants of yeast homologs was conserved (Schmidt et al. 2013). Also, the gene 675

expression of one of the two reil isoforms in each species was activated after shift to low 676

temperatures, namely Arabidopsis reil2 (cf. Supplemental Figure 5 of Schmidt et al. 2013) 677

and yeast rei1 (Strassburg et al., 2010). These findings led us to focus the current study on 678

the cold acclimation process. 679

Our experiments establish cold acclimation of Col-0 WT to 10°C chilling temperature at the 680

vegetative rosette stage, ~1.10 (Boyes et al., 2001), as physiologically relevant and 681

experimentally feasible system for the study of cytosolic RBFs. We confirm increase of reil2 682

mRNA under these conditions (Supplemental Table S2). Successful cold acclimation of Col-683

0 to 10°C starts with a growth arrest of approximately 1 week followed by resumed growth 684

and development (Figure 2), vegetative to the regenerative phase transition, and flowering 685

(Figure 1). The growth arrest coincides with proposed initial inhibition of protein translation 686

after cold shift that appears to be mediated by GENERAL CONTROL NON-687

DEREPRESSIBLE1 (GCN1)/ GCN2 dependent phosphorylation of alpha subunit of 688

eukaryotic translation initiation factor 2, eIF2α, and the TARGET OF RAPAMYCIN (TOR) 689

pathway (Wang et al., 2017). Our data clearly indicate that Arabidopsis physiology is far from 690

inactive during the initial lag phase as is expected according to reports that show 691

requirement of de novo protein synthesis at low temperature. The requirement of active 692

translation after cold shift was demonstrated, for example, by mutants of translation 693

elongation factor 2 (eEF2)-like protein, LOW EXPRESSION OF OSMOTICALLY 694

RESPONSIVE GENES1, LOS1 (Guo et al., 2002) or of Arabidopsis F-BOX PROTEIN7 695

(Calderón-Villalobos et al., 2007). Besides induction of reil2 expression, Col-0 specifically 696

activates expression of genes that encode cytosolic RPs in contrast to the mostly non-697

responsive chloroplast RP genes (Figure 10; Supplemental Table S5). Apparently, the 698

cytosolic translational apparatus is remodeled at the level of structural RP, already 699

characterized RBFs and both, translation initiation and elongation factors (Figure 10). The 700

remodeling of the translational apparatus was confirmed with an expected delay between 701

gene expression maximum and subsequent protein accumulation at the level of ribosome 702



33

subunit and polysome composition (Figure 5D; Figure 10B). Reduced polysome abundance 703

may still support the remodeling process and agrees with the growth arrest. In addition, 704

subunit composition changes dynamically, specifically the relative abundance of the 60S 705

LSU (Figure 5). The cause of the subunit dynamics cannot unambiguously be determined 706

because our current methods do not distinguish between subunit recycling from polysomes 707

and subunit accumulation caused by de novo biosynthesis. Nevertheless, the strong and 708

specific activation of cytosolic RP gene expression and the subsequent relative increase of 709

cytosolic subunits and cytosolic rRNA (Figure 5) support the conclusion that 10°C 710

acclimation of Col-0 involves activation of cytosolic ribosome biogenesis. 711

Cold acclimating reil1-1 reil2-1 remains viable and maintains WT cold acclimation 712

responses 713

We selected the reil1-1 reil2-1 double mutant as object of our systems analyses of 714

Arabidopsis REIL function. Consequently, our current systems analyses cannot differentiate 715

paralog-specific functions. However, we expected that experimental results will be clearer 716

than those of the single mutants, which may have compensatory reactions of the remaining 717

intact paralog. For example, REIL1 deficiency causes no obvious morphological phenotype 718

in reil1-1. REIL1 deficiency can almost completely be compensated by REIL2 (Schmidt et al. 719

2013). In addition, the cold sensitivity of the reil2 mutant growth is restricted only to the 720

vegetative phase (Schmidt et al., 2013). Reil1-1 reil2-1 was the first double homozygous 721

mutant that we obtained and focused on, because reil2-1 has a stronger phenotype 722

compared to reil2-2 (Schmidt et al., 2013). Importantly, the double homozygous reil1-1 reil2-723

2 that was not yet available when we performed the functional complementation and 724

systems analyses of the current study is also strongly growth-impaired in the cold. 725

The strong response of reil1-1 reil2-1 to cold exposure (Figure 1B-D) raised our concern that 726

reil1-1 reil2-1 may exhibit pleiotropic effects that obscure the primary effects of REIL 727

deficiency. Because the reil1-1 reil2-1 mutant is morphologically similar to Col-0 under 728

standard conditions (Figure 1A, 2), we tried to minimize pleiotropic effects by performing shift 729

experiments from standard temperature to cold-conditions. We ruled out inverse temperature 730

shifts as an option (Figure 1E). Inverse temperature shift experiments are not only material 731

limited due to the dwarf-phenotype but are also biased by activation of a rapid flowering 732

program that was reminiscent of stress-induced early flowering (Xu et al., 2014). 733

The next concern was the possibility that reil1-1 reil2-1 cells may be destabilized after cold 734

shift, even though successful temperature rescue experiments demonstrated that the reil1-1 735

reil2-1 mutation is non-lethal in the cold (Figure 1B). Our results indicate that the reil1-1 reil2-736



34

1 phenotype is an arrest or rather a strong retardation of leaf expansion growth and of 737

development of new leaves at low temperature (Figure 1-2). This interpretation is supported 738

by unchanged electrolyte leakage, which unlike the los1-1 mutant (Guo et al., 2002), 739

indicates unaltered stability of the plasma membrane of rosette leaves under both, non-740

acclimated conditions and after cold acclimation (Figure 2C). In addition to the maintained 741

cellular integrity and obviously unchanged acquisition of freezing tolerance, reil1-1 reil2-1 742

also remains physiologically competent of WT cold acclimation responses, both at metabolic 743

(Figure 7) and at transcriptomic levels (Figure 9). For example, transient maltose 744

accumulation is a characteristic acclimation response caused by starch degradation 745

following 4°C cold shock (Kaplan et al., 2004; Kaplan et al., 2007; Maruyama et al., 2009). 746

This hallmark response also occurred after shift to 10°C and was virtually indistinguishable 747

in mutant and Col-0 (Figure 7C). Similarly, transcriptional cold acclimation responses 748

remained largely unaffected. For example, activation of the DREB/CBF-regulon (Yamaguchi-749

Shinozaki and Shinozaki, 2009; Lata and Prasad, 2011), which integrates cold responses 750

and the concurrent water limitation and osmotic responses (Supplemental Figure S6), was 751

highly similar to WT (Figure 9). Even selected vernalization responses were unaffected 752

(Figure 11). 753

Our investigations of reil1-1 reil2-1 obviously show surprisingly limited effects that are largely 754

not confounded by cell death during cold acclimation. Therefore, we concluded that reil1-1 755

reil2-1 represents a valid and feasible system for the functional analysis of Arabidopsis REIL 756

proteins. To demonstrate phenotype rescue we re-introduced REIL1 and REIL2 into the 757

mutant background. Phenotype rescue was achieved using the constitutive UBQ10 promoter 758

and N-terminal FP-fusion proteins (Figure 3). Expression of N-terminal RFP- and GFP- 759

fusion proteins in reil1-1 reil2-1 reconstituted the rosette morphologies of the reil1 or reil2 760

single mutants (Figure 3A-B) and their respective rate of seedling establishment (Figure 3C-761

D). Apparently REIL function has little demand for exact timing and tissue localization of 762

gene expression. Ectopic REIL expression by the UBQ10 promoter caused no observable 763

detrimental effects except for a small delay of the appearance of first rosette leaves at 20°C 764

(Supplemental Figure S2). 765

Arabidopsis REIL proteins reveal conserved and new functional aspects 766

Rescue of reil1-1 reil2-1 phenotype was prerequisite of studies that indicate conserved 767

cytosolic localization of Arabidopsis REIL proteins (Figure 4). REIL1 shows strictly 768

conserved localization and is excluded from nuclei, vacuoles, and chloroplasts (Figure 4). In 769

contrast, REIL2 localization was more divergent and extended into the nucleus of guard cells 770

or the root tip (Figure 4D-F). These observations and the previously reported rescue of the 771



35

yeast ∆rei1 mutant by REIL1 but not by REIL2 (Schmidt et al., 2013) indicate that REIL1 772

may be the more conserved paralog, whereas REIL2 may be a neo-functionalized paralog. 773

Localization of Arabidopsis REIL2 to the nucleus suggests that REIL2 may adopt a 774

conditional function as a pre-60S nuclear assembly and export factor similar to yeast Nog1 775

(Wu et al., 2016). This suggestion requires, however, further validation because we currently 776

cannot rule out tissue or condition specific activation of a paralog selective protease. 777

Protease action may cause local cleavage of RF-fusion proteins so that resulting free RFP 778

may re-localize to the nucleus. 779

Conservation of REIL function is furthermore evident by requirement of REIL proteins for 780

rapid accumulation of cytosolic ribosome subunits after cold shift (Figure 5) and in addition, 781

by association of the REIL1 protein with 60S LSU containing ribosome fractions (Figure 6). 782

In contrast to yeast Rei1 and Reh1 (Hung and Johnson, 2006; Lebreton et al., 2006; Meyer 783

et al., 2007), we also find association of the Arabidopsis REIL1 protein with translating 784

ribosome fractions, e.g. the 80S and polysome fractions (Figure 6). This observation may 785

point towards an additional role of Arabidopsis REIL for the cytosolic translation process or 786

for subunit recycling. Again, further analyses are required, not least because our Western-787

blot analyses indicate a weak and possibly more transient interaction of the REIL proteins 788

with the Arabidopsis 60S LSU than the strong interactions that allow capture of yeast 789

Rei1/Reh1-60S complexes (Greber et al., 2012; Greber et al., 2016; Ma et al., 2017). The 790

case of REIL1 is complicated by proteolysis after density gradient preparation. We can 791

currently not assign functional significance to REIL1 proteolysis. Arabidopsis REIL proteins 792

and their complexes with the 60S LSU clearly need to be stabilized during preparation as a 793

prerequisite for future functional analyses. 794

REIL function is linked to Arabidopsis temperature perception and development 795

Our analyses clearly indicate plant-specific functions of Arabidopsis REIL proteins. 796

Metabolomic and transcriptomic evidence indicates premature triggering of cold acclimation 797

responses in the mutant under standard growth conditions. Non-acclimated reil1-1 reil2-1 798

mimics the metabolic phenotype of 10°C cold acclimating Col-0 (Figure 7 A-B, Supplemental 799

Figure S4) and prematurely triggers the DREB/CBF-regulon with a preference for the cold 800

acclimation factors, CBF1/DREB1B, CBF2/DREB1C, and CBF3/DREB1A, over the heat and 801

osmotic components DREB2A and DREB2B (Figure 8A-B, Figure 9). Indeed, 802

CBF3/DREB1A activation explains the cold-induced carbohydrate metabolism and starch-803

degradation. These metabolic processes are apparently under control of CBF3/DREB1A, but 804

not influenced by DREB2A overexpression in transgenic plants (Maruyama et al., 2009). 805



36

We conclude that either direct REIL function or REIL-dependent availability of translationally 806

competent cytosolic 60S LSUs feedback on Arabidopsis temperature perception. In this 807

feedback loop REIL either directly or indirectly modifies temperature perception by 808

suppressing premature low-temperature acclimation responses. REIL may modulate the 809

energy- and resource-demanding ribosome biogenesis after cold shift. Furthermore, REIL 810

clearly does not operate a ribosome biogenesis switch but rather enhances the kinetics of 811

cytosolic 60S LSU accumulation after cold shift (Figure 5) and the transcriptional activation 812

of cytosolic RPs, RBFs and translation related genes (Figure 10). 813

Besides the likely role of Arabidopsis REILs as kinetic modulators of cold triggered cytosolic 814

ribosome biogenesis, we discovered a link between REILs and vegetative to regenerative 815

phase transition in the cold. REIL proteins are required to trigger transcription of FT mRNA in 816

mature leaves at low temperature conditions (Figure 11). In this context, we suggest that 817

REIL function overrides both FLC-mediated release of inhibition of FT expression and 818

AGL19 dependent activation of FT expression. Altered gene expression of both factors is 819

apparently part of the premature triggering of limited cold responses in non-acclimated reil1-820

1 reil2-1 (Figure 11). REIL action is also apparently required upstream of FLC and AGL19 821

expression and is likely vernalization-independent (Figure 11). We suggest that REIL 822

proteins execute a specific, yet either direct or indirect input into the signaling chain that is 823

required for FT mRNA activation in cold acclimating mature leaves and subsequently for the 824

vegetative to reproductive phase transition of the shoot apical meristem. 825

Conclusion 826

Our current work further establishes REIL proteins as likely RBFs with roles as kinetic 827

modulators of cytosolic ribosome biogenesis or recycling in the cold that may help overcome 828

initial cold induced inhibition of translation (Wang et al., 2017). We also reveal the possibility 829

of functional changes of Arabidopsis REIL proteins during plant evolution and integration of 830

REIL function into plant specific physiological processes such as cold acclimation and flower 831

induction in the cold. We summarize our current conclusions on the role of REIL in 832

Arabidopsis by a functional interaction model (Figure 12). 833



37

Our investigations focused so far on mature leaf tissue as a first source of amply available 834

leaf material for systems analyses. REILs clearly play a role in cold acclimating mature 835

leaves that were already pre-formed at standard temperature. Current results, however, 836

indicate that REIL function may be also important for young leaf or root tissue that grows and 837

develops in the cold. Therefore, future functional investigations may be specifically fruitful 838

when focused on tissues that develop in the cold and on mechanisms that integrate 839

ribosome biogenesis, cell propagation and extension growth. 840

Materials and Methods 841

Plant Material 842

The double homozygous reil1-1 reil2-1 mutant was created by Schmidt and co-authors 843

(2013) by crossing the T-DNA insertion mutant SALK_090487 (reil1-1) that was obtained 844

through the NASC-Nottingham Arabidopsis Stock Centre (Scholl et al., 2000) and 845

GK_166C10 (reil2-1) of the GABI-Kat program (Rosso et al., 2003). T-DNA insertions had 846

been characterized previously by sequencing of the left border insertion sites (Schmidt et al., 847

2013). Homozygosity of the insertion sites was verified by PCR amplification of genomic 848

DNA with previously described T-DNA- and reil1- or reil2-specific oligonucleotides (Schmidt 849

et al., 2013). According to the reported genetic background of the initial mutants, the ecotype 850

Col-0 was used as wild type (WT) control throughout this study. 851

Growth Conditions 852

Generation of seed batches, storage, sterilization and in vitro cultivation was as described 853

previously (Schmidt et al., 2013). Arabidopsis seeds were germinated under sterile 854



38

conditions in long days with a 16 h/8 h day/night cycle and temperature settings as given 855

below using half strength MS-agar plates with 0.8% agar and 2% sucrose (Murashige and 856

Skoog, 1962). Seedlings at stage 1.02-1.03 (Boyes et al., 2001) were transferred, if not 857

mentioned otherwise, to 10 cm diameter pots with Arabidopsis soil (Stender AG, 858

Schermbeck, Germany) after a period of in vitro cultivation that was adjusted to the 859

temperature dependent rate of development. Pots with mutant and WT plants (n ≥ 10) were 860

arrayed on growth chamber shelves in Latin square designs. 861

Constant standard temperature conditions (Figure 1A). Seedlings were transferred to soil 862

after 10 days of in vitro cultivation at 20°C. Plants were acclimated to soil in short days with 863

an 8 h/16 h day/night cycle at 20°C/18°C, 100-150 µmol m-2 s-1 light intensity, and 60%-70% 864

relative humidity using a controlled-environment chamber. After a total of 4 weeks, namely 865

10 days in vitro cultivation and 18 days on soil, the WT reached stage ~1.10. 866

Constant low temperature conditions (Figure 1B). Seedlings were transferred to soil after 867

four weeks in vitro cultivation at 10°C. Plants were acclimated to soil using a controlled-868

environment chamber set to long days with a 16 h/8 h day/night cycle at 10°C/8°C, 100-150 869

µmol m-2 s-1 light intensity, and 60%–70% relative humidity. After acclimation, plant 870

cultivation was continued under identical conditions. WT plants reached stage ~1.10 after a 871

total of 6 weeks, namely 28 days in vitro cultivation and 2 weeks on soil. Care was taken 872

throughout cultivation to maintain plants at 10°C without accidental transient shifts to 873

elevated temperatures. 874

Temperature shift from 20°C to 10°C or 4°C (Figure 1C-D). At stage ~1.10 plants were 875

transferred from standard conditions to a controlled-environment chamber that was set to 876

long days with a 16 h/8 h day/night cycle at 10°C/8°C, 100-150 µmol m-2 s-1 light intensity 877

and 60%-70% relative humidity. The alternative settings were 4°C during both, day and night 878

at ~90 µmol m-2 s-1 light intensity without humidity control. Control plants for temperature 879

shift experiments were moved in parallel to 16 h light of 100-150 µmol m-2 s-1 light intensity at 880

20°C and 8 h night at 18°C with 60%-70% relative humidity. 881

Temperature shift from 10°C to standard temperature conditions (Figure 1C). WT plants at 882

stage ~1.10 and simultaneously co-cultivated mutant plants that had stage 1.02-1.03 were 883

transferred from the 10°C/8°C settings to the 20°C/18°C conditions described above. 884

In vitro Germination and Morphometric Growth Assays 885

In vitro germination assays of Col-0, reil1-1 reil2-1 and complemented reil1-1 reil2-1 were 886

performed and the appearance of first juvenile rosette leaves scored exactly as described 887



39

previously (Schmidt et al., 2013). A 16 h/8 h day/night cycle was applied and either constant 888

20°C or constant 10°C. Strict maintenance of cold-conditions was controlled to ensure full 889

suppression of reil1-1 reil2-1 rosette leaf emergence (Figure 3 C-D, Supplemental Figure 890

S2). 891

Morphometric growth assays, namely measurements of leaf numbers and planar rosette leaf 892

areas (Figure 2A-B), were performed as described previously (Schmidt et al., 2013). Plants 893

were cultivated in single 10 cm diameter pots on soil. Pots were arranged in a Latin square 894

array. Three to ten plants of each genotype, condition and time point were analysed after 895

temperature shifts from 20°C standard conditions to either 10°C or 4°C as described above 896

(Figure 1C-D). Photographs were taken at 4,928 × 3,264 pixel resolution in weekly intervals 897

starting at the time of temperature transfer, i.e. week 0, with a SLR Nikon D5100 camera 898

(Nikon Cooperation, Tokio, Japan), an AF-S DX Nikkor 18 to 55 mm, F/3.5-5.6 VR lens, and 899

a 1.0 mm resolution scale on each photograph. Images were normalized to scale and 900

analysed with manual supervision using Adobe Photo Shop CS5 Extended (Adobe 901

Photoshop Version 11.0, Adobe Systems, San Jose, California, USA). 902

Electrolyte Leakage Assays 903

Electrolyte leakage measurements of cellular integrity and assessment of acquired freezing 904

tolerance (Figure 2C) was according to previously published standardized protocols (Rohde 905

et al., 2004; Thalhammer et al., 2014). Tubes with 3 stacked mature leaves or up to half a 906

rosette to match equal leaf amounts were placed in test tubes with a bottom layer of double 907

distilled water and kept at 4°C on ice. Tubes with non-frozen control samples were 908

maintained on ice to determine the basal electrolyte content. Test tubes for the freezing 909

assays were transferred to a cooling bath, equilibrated 30 min at -1°C, and ice nucleation 910

initiated for a subsequent 30 min period (Thalhammer et al., 2014). Test tubes were then 911

cooled at a rate of 4°C/h. Four to eight samples per 1°C temperature interval were removed 912

from the bath and immediately placed on ice. All frozen and non-frozen control samples 913

were kept together overnight on ice in a 4°C chamber and then diluted by double distilled 914

water. Paired electrical conductivities of leaked electrolytes from initially non-boiled samples 915

and total electrolyte content from subsequently boiled samples were determined. The 916

percentage of electrolyte leakage was calculated and normalized to the electrolyte content of 917

non-frozen control samples. The LT50 value, i.e. the temperature of 50% normalized 918

electrolyte leakage, was calculated by the LOGEC50 value of sigmoidal fitted curves using 919

the GraphPad Prism 3.0 software (Thalhammer et al., 2014). 920

Sodium Dodecylsulfate-Polyacrylamide Gel Electrophoresis (SDS-PAGE) and Western 921

Blot Analysis 922



40

One hundred mg of liquid nitrogen flash-frozen and ground leaf material were extracted in 923

denaturing SDS-loading buffer that contained 50 mM Tris-HCl at pH 6.8, 4% SDS, 30% 924

glycerol, 0.1 M dithiothreitol, 0.05% bromophenol blue, and cOmpleteTM protease inhibitor 925

(Sigma-Aldrich, St. Louis, MO, USA) at a dose of 1 tablet per 1.5 mL extraction buffer. 926

Western blot analysis was conducted as described previously (Grefen et al., 2009) after 927

separation of 18 µL total protein in loading buffer at a 0.2 mg µL-1 concentration by 12% 928

acrylamide SDS-PAGE. 929

REIL-specific, 14-amino acid, polyclonal peptide antibodies with an additional N-terminal 930

cysteine leader for carrier protein conjugation were epitope-selected by the 931

OptimumAntigenTM design tool (GenScript Inc., Piscataway, NJ, USA) and obtained from the 932

same company. The anti-atREIL1.1 antigen-peptide was (C)MSKRGETMRTKIGV 933

representing amino acid positions 377-390 of REIL1, C-terminal positions -28 to -15. Anti-934

atREIL2.1 was directed against (C)KRTDNKVTSRTLGS equivalent to amino acid positions 935

305-318 of REIL2, C-terminal positions -91 to -78. The red fluorescent protein specific 936

polyclonal antibody (anti-RFP) was obtained from Abcam PLC (Cambridge, UK, 937

http://www.abcam.com). Polyclonal anti-RPL13B antibodies (AS13 2650/anti-L13-1) directed 938

against the ~23.8 kDa RPL13B 60S subunit protein encoded by At3g49010 (Barakat et al., 939

2001; Sormani et al., 2011), were obtained from Agrisera AB (Vännäs, Sweden). Anti-RFP, 940

anti-RPL13B, and anti-atREIL1.1 were used at 1:5000, anti-atREIL2.1 at 1:3000 dilutions. 941

The primary antibodies were detected by an anti-rabbit immunoglobulin G-horseradish 942

peroxidase secondary antibody that was diluted 1:10000. Protein-antibody complexes were 943

visualized by enhanced chemiluminescence (ECL) reagents (ThermoFisher Scientific Life 944

Technologies GmbH, Darmstadt, Germany). Western blots were analyzed by the G:BOX F3 945

automated gel imaging system (Syngene, Cambridge, UK) and processed with the Molecular 946

Analyst™ image analysis software (Bio-Rad Laboratories Inc., Hercules, CA, USA). 947

Construction of FP-REIL reporter lines 948

All expression vectors were cloned and amplified by Gateway recombination cloning 949

technology (Earley et al. 2006, Grefen et al. 2010). Clones containing reil genes were 950

constructed after polymerase chain reaction (PCR) amplification of complementary DNA 951

(cDNA) from reverse transcribed messenger RNA (mRNA) using the Sal1 and Not1 952

restriction sites of the pENTRTM 1A vector and transformed into TOP10 competent E. coli 953

cells (Invitrogen Life Technologies GmbH, Darmstadt, Germany). Successful cloning events 954

were verified by colony PCR and sequencing of prepared vector DNA (LGC Genomics 955

GmbH, Berlin, Germany). GatewayTM vectors were cloned and amplified by E. coli ccdB 956

SurvivalTM cells (Invitrogen Life Technologies GmbH, Darmstadt, Germany), and selected by 957



41

50 µg mL-1 spectinomycin and 25 mg mL-1 chloramphenicol. Vectors with the expression 958

cassettes UBQ10::GFP-REIL1, UBQ10::RFP-REIL1, UBQ10::GFP-REIL2, UBQ10::RFP-959

REIL2, and UBQ10::REIL2 were placed under control of the Arabidopsis UBIQUITIN 10 960

promoter (UBQ10, AT4G05320) using the site-specific recombination sites attB1 and attB2. 961

The LR recombination reaction included a mixture of 150 ng pUBN-GFP-DEST or pUBN-962

RFP-DEST vectors (Grefen et al., 2010; https://www.uni-tuebingen.de/en/faculties/faculty-of-963

science/departments/interdepartmental-centres/center-for-plant-molecular-biology/dev-964

genetics/grefen/resources/ubiquitin10-vectors.html), 150 ng of the pENTRTM clones with the 965

respective reil genes and 0.5 μL LR-clonase II (Invitrogen Life Technologies GmbH, 966

Darmstadt, Germany). 967

Vectors were transformed into reil1-1 reil2-1 mutant plants (Schmidt et al., 2013) by 968

Arabidopsis in planta Agrobacterium transformation (Bent et al. 2000). UBQ10::GFP(RFP)-969

REIL reporter lines in reil1-1 reil2-1 mutant background were screened at T1 generation by 970

50 mg mL-1 BASTA (glufosinate) herbicide MS plates. Resistant seedlings were selected at 971

cotyledon stage for generation of the T2 generation. Segregation of the T2 generation was 972

checked after 30 days in vitro cultivation at 10°C. Homozygous individuals were selected at 973

stage 1.02-1.04, tested positively for expression of protein fluorescence, and were 974

transferred to soil for seed batch propagation under standard greenhouse conditions. 975

Polymerase Chain Reactions (PCR) 976

PCR was performed with 36 cycles, 15 s denaturation at 94°C followed by 30 s annealing at 977

55°C and 2 min elongation at 72°C, using total RNA that was extracted using the RNeasy 978

Plant Mini Kit (QIAGEN GmbH, Hilden, Germany). cDNA was synthesized from total RNA by 979

SuperScript® II Reverse Transcriptase (Invitrogen Life Technologies GmbH, Darmstadt, 980

Germany). The reil1-1 reil2-1 mutant background was verified by T-DNA specific forward 981

oligonucleotide primers, LBb1 (SALK) and GKo8409 (GABI-Kat), and reil gene specific 982

reverse primers, refer to Supplemental Table S5 of Schmidt et al. (2013). The forward and 983

reverse oligonucleotide primers for the verification of the presence of the expression 984

cassettes were nGFPfor 5´-AAGGGCGAGGAGCTGTT-3´ (UBQ10::GFP-REIL1), nRFPfor 985

5´-GAGGACGTCATCAAGGAGT-3´ (UBQ10::RFP-REIL1) combined with 3´-non-coding 986

REIL1_at4g31420rev2 5´-GTGCGGCCGCAAGTGGCACATACACAG-3´ or nGFPfor 5´-987

AAGGGCGAGGAGCTGTT-3´ (UBQ10::GFP-REIL2), nRFPfor 5´-988

GAGGACGTCATCAAGGAGT-3´ (UBQ10::RFP-REIL2), and REIL2_at2g24500for2 5´-989

GCGTCGACGATGTCAGGTTTAGCTTGT-3´ (UBQ10::REIL2) combined with 990

REIL2_at2g24500rev2 5´-GTGCGGCCGCGAAAATCGAGGAGCAAGA-3´, respectively. 991

Fluorescence microscopy for FP-REIL protein localization. 992



42

Seeds of functionally complemented FP-REIL reporter lines UBQ10::RFP-REIL1 (line 49) 993

and UBQ10::RFP-REIL2 (line 109) were germinated and grown in vitro as described above. 994

Fluorescence microscopy of biological replicates of root tips and cotyledons from 3-5 995

individual plants was performed after 7-10 d growth at 20°C or 7 days after subsequent shift 996

to 10°C. To visualize subcellular localization of RFP fluorescence, a Leica TCS SP5 997

confocal laser scanning microscope was used with a 63X objective. Projection stacks of 998

multiple confocal sections, overlays, and false color renderings were generated using the 999

manufacturer´s LSM software (Leica Microsystems GmbH, Wetzlar, Germany). RFP 1000

excitation was achieved using a 561 nm laser. Emission was monitored between 572 nm 1001

and 634 nm. Chlorophyll fluorescence was obtained using the same excitation settings but 1002

emission spectra were recorded in the range 652 nm to 727 nm. 1003

Microfluidic electrophoresis-based analysis of relative rRNA abundance 1004

Relative abundance of cytosolic and chloroplast rRNA species was determined by 1005

microfluidic electrophoresis using an Agilent 2100 Bioanalyzer and the Agilent RNA 6000 1006

Nano Kit according to manufacturer´s instructions (Agilent Technologies GmbH & Co. KG, 1007

Waldbronn, Germany). Samples of total RNA were extracted from 50 mg fresh weight (FW) 1008

of mature rosette leaves by the TRIzol reagent method (Ambion GmbH, Kaufungen, 1009

Germany). rRNA ratios determined as described previously (Walter et al., 2010; Salvo-1010

Chirnside et al., 2011). Four biological replicates that represent preparations from 1011

independent pools of ≥ 2 plants, with 2 technical repetitions each, were analyzed per 1012

genotype and temperature condition. 1013

Density gradient analysis of Arabidopsis ribosomes 1014

Ribosome fractions were isolated from three independent pools of mature Arabidopsis 1015

leaves from ≥ 2 plants that were harvested at approximately 6 h +/- 0.5 h after dawn 1016

according to Kawaguchi et al. (2004) and Piques et al. (2009) with minor modifications. 1017

Briefly, 100 mg frozen leaf tissue was homogenized 30 min on ice in 0.5 mL of polysome 1018

extraction buffer (PEB), i.e. 200 mM Tris-HCl, pH 9.0, 200 mM KCl, 25 mM EGTA, 36 mM 1019

MgCl2, 5 mM dithiothreitol (DTT), with 50 μg mL−1 cycloheximide, 50 μg mL−1 1020

chloramphenicol, 0.5 mg mL−1 heparin, 1% (v/v) Triton X-100, 1% (v/v) TWEEN 20, 1% (w/v) 1021

Brij-35, 1% (v/v) IGEPAL CA-630, 2% (v/v) polyoxyethylene, and 1% (w/v) deoxycholic acid 1022

(Sigma-Aldrich, St. Louis, MO, USA). All procedures were carried out at 4°C. After 1023

clarification by centrifugation at 14,000g for 10 min, hydrated tissue was placed on a 1024

QIAshredder spin column of the RNeasy Plant Mini Kit (Qiagen, Hilden, Germany) and 1025

centrifuged at 14,000g for 1 min to remove cell debris. Volumes of 0.5 mL extract were 1026

loaded onto 9 mL of a 15%-60% sucrose gradient cushion. The loaded gradient was ultra-1027



43

centrifuged at 30,000g for 18 h at 4°C in a six-bore SW 41 Ti rotor (Beckman, Fullerton, CA, 1028

USA). 1029

One analysis run comprised a set of 6 samples, 2x2 or 4x1 independently extracted 1030

replicates of the investigated conditions and 2 fixed control samples, namely a non-sample 1031

control with empty extraction buffer and a positive control prepared from a previously 1032

harvested and long-term stored homogenous reference batch of Col-0 rosette leaves. This 1033

reference batch was generated at developmental stage ~1.10 from plants that were 1034

cultivated at standard temperature conditions. The sucrose gradients were separated into 40 1035

fractions of approximately 250 µL by a programmable density gradient fractionation system 1036

(Teledyne Isco Inc., Lincoln, NE, USA), which recorded a continuous absorbance profile at 1037

254 nm. After quality control of the Col-0 reference sample profile, absorbance profiles were 1038

exported and background subtracted by the non-sample control profile. Areas of ribosome 1039

fractions and total absorbance were determined by Cromas Lite 2.1 software 1040

(http://chromas-lite.software.informer.com/2.1/). To account for variations of loaded sample 1041

amounts, ribosome areas were normalized through division by total peak area. 1042

Identification and Western blot analysis of ribosome fractions 1043

Ribosomal fractions were located within the profiles by screening of the whole sucrose 1044

density profile range. All 40 fractions were analyzed by 1.2% agarose gel electrophoresis of 1045

TRIzol total RNA preparations. rRNA containing fractions were chosen for microfluidic 1046

electrophoresis (Salvo-Chirnside et al., 2011) and qualitative analysis of rRNA species (e.g. 1047

Figure 5, Supplemental Figure S3), with cytoplasmic 25S and 18S rRNA and chloroplast 23S 1048

and 16S rRNA annotations according to Nishimura et al. (2010) and Tiller et al. (2012). 1049

For Western blotting, complete 250 µL sucrose density gradient fractions were precipitated 1050

by 600 µL of 100% (v/v) methanol, 150 µL of chloroform and 400 µL H2O. After a short 1051

vortex step and 10 min centrifugation at 14,000g the upper layer was carefully removed and 1052

a second washing step with 650 µL of methanol performed. The final centrifugation was 20 1053

min at 14,000g. The collected pellet was suspended in 24 μL SDS-PAGE loading buffer and 1054

Western blot analysis continued as described above. 1055

Systems analyses 1056

Sampling. Samples for paired metabolome and transcriptome analyses were prepared from 1057

Arabidopsis Col-0 and reil1-1 reil2-1 mutant plants at stage ~1.10 that were transferred 6 h 1058

after the start of the light period from the 20°C conditions to the 10°C regime described 1059

above. Mature leaves were harvested at 0 h, i.e. non-acclimated, before transfer and 0.25, 1060



44

0.50, 1, 2, 4, 8, 24, 48, and 72 h after transfer as well as at 1, 2, 3 and 4 weeks after 1061

transfer. Daily and weekly samplings were all at approximately 6 h after dawn. Three 1062

replicate samples each were collected in two independent experiments and immediately 1063

frozen in liquid nitrogen. Each replicate sample was a pool of mature leaf material from at 1064

least two rosettes. Leaf tissue was frozen in liquid nitrogen immediately after harvest. 1065

Gas chromatography-mass spectrometry (GC-MS)-based metabolome analysis. All collected 1066

leaf material was ground and weighed in the frozen state and a polar metabolite fraction 1067

extracted by standardized methanol/chloroform/water extraction and liquid phase separation 1068

as described previously (Roessner et al. 2000, Dethloff et al. 2014). The polar metabolite 1069

fraction was methoxyaminated and trimethylsilylated and GC-MS profiling performed by 1070

electron impact ionization/time-of-flight mass spectrometry using an Agilent 6890N24 gas 1071

chromatograph (Agilent Technologies, Böblingen, Germany; http://www.agilent.com) and a 1072

Pegasus III time-of-flight mass spectrometer (LECO Instrumente GmbH, Mönchengladbach, 1073

Germany). GC-MS peak abundances (responses) were processed into a standardized 1074

numerical data matrix that was normalized by sample FW and internal standard, U-13C-1075

sorbitol. Metabolites annotated using the TagFinder software (Luedemann et al., 2008) by 1076

mass spectral and retention time index matching to the reference collection of the Golm 1077

metabolome database (GMD), http://gmd.mpimpgolm.mpg.de (Kopka et al., 2005; Hummel 1078

et al., 2010) and to the mass spectra of the NIST database 1079

(http://www.nist.gov/srd/mslist.htm). Normalized metabolite response ratios were calculated 1080

per metabolite relative to the measurement of non-acclimated Col-0 and log2-transformed. 1081

Microarray transcriptome analysis. Total plant RNA of samples from the time points 0 (non-1082

acclimated, i.e. before transfer), 1 day, 1 week, and 3 weeks was isolated from leaf tissue 1083

that was paired back-up material of the metabolome study using the RNeasy Plant Mini Kit 1084

and RNase free DNAse (Qiagen, Hilden, Germany). Three replicate samples, and in the 1085

case of non-acclimated plants, five to six replicate samples that represented independent 1086

pools of mature rosette leaves from two or three plants were analyzed. RNA integrity number 1087

(RIN) was calculated by microfluidic electrophoresis using an Agilent 2100 Bioanalyzer and 1088

2100 Expert software (Agilent Technologies GmbH & Co. KG, Waldbronn, Germany). RNA 1089

samples with RIN > 8.0 were sent to the 4×44K Agilent expression profiling service of 1090

ATLAS Biolabs GmbH (Berlin, Germany). Gene expression data sets were quantile 1091

normalized using the “normalize.quantile” routine of the “preprocessCore” R statistical 1092

computing and graphics package (https://www.r-project.org/). The 4×44K Agilent expression 1093

profiling microarray contains variable numbers of redundant gene probes. Gene expression 1094

information was averaged if redundant probes were present to avoid bias of functional 1095

enrichment analyses. Gene expression information was normalized per gene to non-1096



45

acclimated Col-0. Alternatively, the differential gene expression of mutant over Col-0 was 1097

calculated at each time point. Mode of normalization is indicated within legends and table 1098

headers (Supplemental Table S2). 1099

Statistical analyses and data visualizations. Quantile normalized log2-transformed ratios of 1100

differentially expressed genes or differentially accumulated metabolites were analyzed and 1101

visualized by Microsoft Excel software of the Office Professional Plus 2010 package 1102

(Microsoft Corporation, Redmond, Washington, USA), by the Multiple Experiment Viewer 1103

(MeV version 4.9.0, http://www.mybiosoftware.com/mev-4-6-2-multiple-experiment-1104

viewer.html) and by MetaGeneAlyse version 1.7.1 (http://metagenealyse.mpimp-1105

golm.mpg.de/). Significance thresholds (P) of statistical analyses were: 1-way and 2-way 1106

ANOVA, P < 0.001; Kruskal-Wallis test, P < 0.001; heteroscedastic t-test, P < 0.01. All 1107

calculated P values are reported within the supplemental information (Supplemental Table 1108

S1, Supplemental Table S2). Details of the data reduction and visualization methods, 1109

namely hierarchical cluster analysis (HCA) and principal component analysis (PCA) are 1110

reported in the legends to the figures and tables. 1111

Functional enrichment analyses of gene expression data. Functional enrichment analysis of 1112

differential gene expression by parametric analysis of gene set enrichment (PAGE, Du et al., 1113

2010), singular enrichment analysis (Du et al., 2010), and visualizations were performed at 1114

agriGO (http://bioinfo.cau.edu.cn/agriGO). Singular enrichment analysis investigates user-1115

defined gene sets without consideration of numerical gene expression levels and provides 1116

information on enrichment of GO categories among these genes (Du et al., 2010). The 1117

PAGE processes lists of genes with log2-transformed numerical differential gene expression 1118

values from one or more experimental conditions. PAGE provides information on enrichment 1119

of either expression increases or decreases across gene sets of GO terms. Additional and 1120

confirmatory enrichment analyses of gene expression was done by MapMan version 3.5.0 1121

(http://mapman.gabipd.org/web/guest/pageman) using the functional bins (equivalent to GO 1122

terms) that were defined by the MapMan and PageMan software developers (Thimm et al., 1123

2004; Usadel et al. 2006). 1124

Accession Numbers 1125

The expression data sets were uploaded to the Gene Expression Omnibus (GEO, 1126

https://www.ncbi.nlm.nih.gov/geo/) and are made available through accession GSE101111. 1127



46

Supplemental Material 1128

Supplemental Tables 1129

Supplemental Table S1 (Excel file): Metabolite profiles and statistical data analyses of the 1130

non-acclimated and 10°C cold acclimating reil1-1 reil2-1 mutant compared to Col-0 WT. 1131

Supplemental Table S2 (Excel file): Gene expression profiles and statistical data analyses 1132

of mature leaves from the non-acclimated and 10°C cold acclimating reil1-1 reil2-1 mutant 1133

compared to Col-0 WT. 1134

Supplemental Table S3 (Excel file): Differentially expressed, shared genes (DEGs) 1135

between the non-acclimated reil1-1 reil2-1 mutant and cold acclimating Col-0 at 1 day, 1 1136

week, or 3 weeks after shift to 10°C. 1137

Supplemental Table S4 (Excel file): Functional enrichment analysis of differential gene 1138

expression in the non-acclimated and cold acclimating reil1-1 reil2-1 mutant at 1 day, 1 1139

week, or 3 weeks after shift to 10°C compared to non-acclimated and cold acclimating Col-0. 1140

Supplemental Table S5 (Excel file): Differential gene expression of ribosome or translation 1141

related genes in the non-acclimated and cold acclimating reil1-1 reil2-1 mutant. 1142

Supplemental Table S6 (Excel file): Differential expression of 64 genes that were 1143

significantly changed more than 4-fold at least once in the non-acclimated or cold 1144

acclimating reil1-1 reil2-1 mutant and selected flowering and vernalization related genes. 1145

Supplemental Figures 1146

Supplemental Figure S1: Characterization of the UBQ10::GFP(RFP)-REIL reporter lines of 1147

the reil1-1 reil2-1 mutant. 1148

Supplemental Figure S2: Comparison of early seedling development at 20°C to 10°C after 1149

constitutive expression of GFP-REIL and RFP-REIL fusion proteins under control of the 1150

UBQ10 promoter in reil1-1 reil2-1. 1151

Supplemental Figure S3. Sucrose density gradient separation optimized for the separation 1152

of the 50S and 60S ribosome fraction from Arabidopsis leaves. 1153

Supplemental Figure S4. Comparison of leaf primary metabolite profiles from non-1154

acclimated reil1-1 reil2-1 to the Col-0 time course of 10°C cold acclimation. 1155



47

Supplemental Figure S5. Correlation analysis of gene expression in non-acclimated reil1-1 1156

reil2-1 at standard cultivation temperature compared to cold acclimating Col-0 at 1 day, 1 1157

week, or 3 weeks after shift to 10°C. 1158

Supplemental Figure S6. Functional enrichment analysis of differential gene expression in 1159

reil1-1 reil2-1 at standard cultivation temperature compared to Col-0 and reil1-1 reil2-1 at 1 1160

day (1 d), 1 week (1 w), or 3 weeks (3 w) after shift to 10°C. 1161

1162

Acknowledgements 1163

We acknowledge the longstanding support by Prof. Dr. L. Willmitzer, Prof. Dr. M. Stitt and 1164

Prof. Dr. R. Bock (Max-Planck-Institute of Molecular Plant Physiology, Potsdam, Germany) 1165

and funding by the Max-Planck Society. We thank the National Council for the Improvement 1166

of Higher Education - CAPES of Brazil for the scholarship provided to A. A. Pereira Firmino. 1167

1168

Figure Legends 1169

Figure 1. Developmental phenotypes of the reil1-1 reil2-1 mutant under standard 1170 and suboptimal temperature regimes. Reil1-1 reil2-1 and Arabidopsis Col-0 WT were 1171 compared under constant temperature and temperature-shift regimes. 1172 (A) Constant standard temperature conditions at 20°C/18°C (day/night). Mutant and WT 1173

reached vegetative developmental stage ~1.10 (Boyes et al., 2001) approximately 1174 four weeks after transfer to soil. Note that the mutant had a mild pointed leaves 1175 phenotype (Van Lijsebettens et al., 1994; Horiguchi et al., 2011). 1176

(B) Constant low temperature conditions at 10°C/8°C (day/night). Mutant plants survived 1177 at least 13 weeks after germination and transfer to soil but remained extremely 1178 dwarfed with final rosette diameters <1 cm and only 5-7 visible leaves. 1179

(C) Temperature shift from the 20°C to the 10°C regime. In contrast to the acclimating 1180 WT, growth and development of the mutant were arrested. Mutant plants survived at 1181 least 13 weeks at low temperatures. 1182

(D) Temperature shift from the 20°C to a 4°C/4°C (day/night) regime. Mutant plants and 1183 WT were growth arrested. Mutant survival was not tested. 1184

(E) Inverse temperature shift from the 10°C to the 20°C regime. In contrast to the de-1185 acclimated WT, mutant plants entered a rapid flowering program reminiscent of 1186 stress-induced early flowering (Xu et al., 2014). 1187

Temperature shifts, C and D, were performed at developmental stage ~1.10 of WT and 1188 mutant at the stages shown by Figure 1A at week 0. Note that plant age is given by week 1189 prior or post developmental stage ~1.10. Plants were germinated under sterile conditions 1190 (Schmidt et al. 2013) and transferred to soil at stage 1.02-1.03, i.e., at -6 weeks (10°C) or -4 1191 weeks (20°C). The inverse temperature shift from 10°C to 20°C (scheme E) was performed 1192 when WT reached stage ~1.10 at 10°C. Co-cultivated mutant plants had stage 1.02-1.03. 1193 Arrow heads within the experimental schemes indicate the time at which representative 1194 photographs of n ≥ 10 plants per experiment were taken. Scale bars are 1 cm. 1195



48

1196 1197 Figure 2. Morphometric and electrolyte leakage assays of reil1-1 reil2-1 at low 1198 temperatures. Reil1-1 reil2-1 and ArabidopsisCol-0 WT were compared after shift from 1199 20°C to either 10°C (left) or 4°C (right). 1200 (A) Leaf number. Mutant and WT differed significantly after 2 weeks at either 10°C or 1201

4°C (P < 0.05; means +/- standard deviations of n = 3 - 10 plants). 1202 (B) Rosette area. Mutant and WT differed significantly after 2 weeks at either 10°C or 1203

4°C (P < 0.05; means +/- standard deviations of n = 3 -10 plants). 1204 (C) Electrolyte leakage assay for the quantitative assessment of freezing tolerance. The 1205

mutant did not show increased electrolyte leakage compared to Col-0 (* indicates P < 1206 0.05; means +/- standard error of n = 4 - 8 pools of leaves). 1207

Experimental designs were according to schemes C and D (Figure 1). Mutant and WT plants 1208 were shifted at developmental stage ~ 1.10 (Boyes et al., 2001). Week 0 plants were 1209 cultivated at 20°C and assayed immediately before temperature shift. Significance was 1210 tested using the heteroscedastic t-test. 1211 1212 1213 Figure 3. Constitutive expression of GFP-REIL and RFP-REIL fusion proteins under 1214 control of the UBQ10 promoter in reil1-1 reil2-1 restores single mutant morphology 1215 and development. Seedling development and vegetative rosette morphology of 1216 representative reil1-1 reil2-1 transformation events using the constructs UBQ10::GFP-REIL2 1217 (b), UBQ10::RFP-REIL2 (c), UBQ10::GFP-REIL1 (e), and UBQ10::RFP-REIL1 (f) were 1218 compared to reil1-1 (a) and reil2-1 (d) plants. 1219 (A) Seedlings after in vitro germination and cultivation at 10°C. Representative 1220

photographs of n ≥ 10 in vitro grown plants per genotype were taken 30 days after 1221 imbibition (cf. C-D). 1222

(B) Rosette plants after in vitro germination at 10°C and constant temperature cultivation 1223 on soil at 10°C/8°C (day/night) according to cultivation scheme B (Figure 1). 1224 Representative photographs of n ≥ 10 plants per genotype were taken 6-7 weeks 1225 after transfer to soil. Racks of 6 cm square pots were used. 1226

(C) Appearance of the first juvenile rosette leaves after introduction of REIL2 fusion 1227 proteins into reil1-1 reil2-1 (means +/- standard deviations of n = 4-5 plates per 1228 genotype. Each plate had ~80 seeds). 1229

(D) Appearance of the first juvenile rosette leaves after introduction of REIL1 fusion 1230 proteins into reil1-1 reil2-1 (means +/- standard deviations of n = 4-5 plates per 1231 genotype. Each plate had ~80 seeds). 1232

Leaf appearance was scored using the 10°C in vitro germination and cultivation assay 1233 described by Schmidt et al. (2013). The analysis included the reil1-1 reil2-1 mutant that is 1234 strongly delayed for the appearance and development of rosette leaves. The arrows indicate 1235 absence of the 1st rosette leaf (cf. Figure 1B), Arabidopsis Col-0 WT, and a non-fusion 1236 protein control, namely UBQ10::REIL2 transformed into reil1-1 reil2-1 (cf. C). Introduction of 1237 REIL1 restored reil2-1 morphology. Introduction of REIL2 restored reil1-1 morphology. Note 1238 that reil1-1 morphology is virtually indistinguishable from WT (Schmidt et al. 2013). 1239 1240 1241 Figure 4. Subcellular fluorescence localization of RFP-REIL fusion proteins. The 1242 UBQ10::RFP-REIL1 (49) and UBQ10::RFP-REIL2 (109) transformation events of reil1-1 1243 reil2-1 that restored respective single mutant phenotypes (cf. Figure 3) were analyzed using 1244 seedlings 7-10 days after germination at standard temperature (20°C) and after ≥ 1 day in 1245 the cold (10°C). 1246

(A) Cotyledon epidermis of UBQ10::RFP-REIL1 (49) after in vitro germination and 1247 cultivation at 20°C. 1248



49

(B) Root tip meristem to transition zone of UBQ10::RFP-REIL1 (49) after in vitro 1249 germination and cultivation at 20°C. 1250

(C) Root tip of UBQ10::RFP-REIL1 (49) after in vitro germination at 20°C and cold shift. 1251 (D) Cotyledon epidermis of UBQ10::RFP-REIL2 (109) after in vitro germination and 1252

cultivation at 20°C. 1253 (E) Root tip of UBQ10::RFP-REIL2 (109) after in vitro germination and cultivation at 1254

20°C. 1255 (F) Root tip of UBQ10::RFP-REIL2 (109) after in vitro germination at 20°C and cold shift. 1256 Representative analyses include (left to right): false color image of RFP fluorescence 1257 (green), Nomarsky Differential Interference Contrast (DIC) image, and overlay including false 1258 color image of chlorophyll auto-fluorescence (red). All images are projection stacks of 1259 multiple confocal sections. Scale bars are 25 µm. Note absence of RFP-REIL1 fluorescent 1260 signal from vacuolar, chloroplast and nuclear lumen (A-C). 1261

1262

Figure 5. Relative abundance of rRNAs within total RNA preparations and of 60S and 1263 50S large ribosomal subunits from total ribosome preparations before and after shift 1264 to 10°C. Complete reil1-1 reil2-1 rosettes were compared to WT (Col-0) in the non-1265 acclimated state, i.e. at 0 days, and at 1, 7, and 21 days (d) after transfer to the cold, 1266 cultivation scheme C (Figure 1). 1267 (A) Ratio of the cytosolic 25S large subunit rRNA relative to chloroplast 23S rRNA (P = 1268

0.001). 1269 (B) Ratio of the cytosolic small subunit 18S rRNA relative to chloroplast 16S rRNA (P = 1270

0.003). 1271 (C) Ratio of cytosolic 25S large subunit rRNA and cytosolic 18S small subunit rRNA (A-1272

C; means ± standard error, n = 3-4 preparations from independent pools of mature 1273 rosette leaves). 1274

(D) Representative sedimentation profiles of total ribosome preparations from ~100 mg 1275 FW of rosettes sampled at day 0, 1, and 7 of acclimation to 10°C. The sedimentation 1276 analysis was optimized for the separation of the 50S to 60S fractions. Indicated 1277 fractions were monitored by blank gradient subtracted absorbance (A254nm). Fraction 1278 identity was verified by rRNA analysis (Supplemental Figure S3). 1279

(E) Analysis of ribosome sedimentation profiles exemplified in (D) by calculating the 1280 normalized A254 nm abundance of the 60S and 50S fractions relative to the sum of all 1281 observed fractions (means ± standard error, n = 3 preparations from independent 1282 pools of mature rosette leaves). 1283

(F) Ratio of the 60S fraction relative to the 50S fraction calculated from the data set of 1284 (E-F) (means ± standard error, n = 3 preparations from independent pools of mature 1285 rosette leaves). 1286

The experimental design was according to scheme C (Figure 1). Mutant and WT plants were 1287 shifted at developmental stage 1.10. Non-acclimated rosettes were cultivated at 20°C and 1288 assayed immediately before temperature shift. Peak areas of rRNA were determined from 1289 total RNA extracts by microfluidic electrophoresis. 23S rRNA was determined by the sum of 1290 two naturally occurring post-maturation cleavage products. (A-B) Significance (P) of the time 1291 effect was tested by 2-way analysis of variance (ANOVA). (E-F) * indicates significant 1292 change of mutant compared to WT (P< 0.05, heteroscedastic t-test). 1293 1294 1295 Figure 6. Western blot analysis of Col-0 ribosome fractions. Ribosome protein fractions 1296 from Col-0 WT were compared to total protein preparations from Col-0 (WT) and reil2.1. All 1297 preparations were from rosette plants of stage ~1.10 that were cultivated at 20°/18°C (day/ 1298 night). 1299



50

(A) Absorbance profile of the sucrose density sedimentation gradient analysis at 1300 wavelength λ = 254 (A254) after blank gradient subtraction. Vertical lines indicate the 1301 approximate positions of collected protein fractions. 1302

(B) Western blot analyses of indicated fractions using anti-atREIL1.1 (top) and anti-1303 RPL13B antibodies (below). Note that anti-atREIL1.1 was directed against a variable 1304 region at the REIL1 C-terminus. This antibody detects REIL1 in total protein extracts 1305 (black arrow) and cleavage products (gray arrows) in protein preparations after 1306 sucrose density gradient centrifugation. Cleavage products are also detectable at low 1307 abundance in total protein from the reil2.1 mutant. The Western analysis was 1308 performed by three parallel-processed blots of fractions from the sedimentation 1309 gradient shown in (A). The anti-RPL13B analyses were of an independent 1310 sedimentation gradient. Splice sites of blots are indicated by white bars. 1311

1312 1313 Figure 7. Relative changes of leaf primary metabolites in the non-acclimated and the 1314 10°C cold acclimating reil1-1 reil2-1 mutant compared to Col-0 WT. 1315 (A) Heat map of relative changes compared to non-acclimated Col-0 (*). Mean ratios 1316

were log2-transformed and color-coded according to inserted scale (n = 6). 1317 Metabolites presented in panel C are indicated (x). Metabolites were arranged by 1318 hierarchical clustering using Euclidian distance and complete linkage. 1319

(B) Principal component analysis (PCA) of the data set shown in panel A. Col-0 in the 1320 non-acclimated state is indicated by * within the 0.00 h circle to the left. The gray 1321 arrow indicates the progressing metabolic changes of Col-0 in the course of cold 1322 acclimation. The black arrow indicates non-acclimated reil1-1 reil2-1. Time after cold 1323 shift is coded by circle size. The 4 d annotation indicates the time point of reil1-1 1324 reil2-1 divergence from WT. 1325

(C) Comparative time course of selected metabolite pools normalized to non-acclimated 1326 Col-0 indicated by *within the 0.00 h circle to the left (means +/- standard error, n = 1327 6). 1328

Plants were pre-cultivated at 20°C and shifted to 10°C conditions at developmental stage 1329 ~1.10 according to scheme C (Figure 1). Samples were harvested immediately before (0.00 1330 h) and following cold shift. Cold shift and sampling time points at full days (d) or weeks (w), 1331 except samplings at 0.25 - 8 h, were at 6 h (+/- 5 min) after dawn of a 14 h/10 h day night 1332 cycle. Two independent experiments with 3 replicate samples each per time point were 1333 performed. Samples were pools of mature leaves from at least two plants. Metabolism was 1334 profiled by multi-targeted GC-MS based technology. Metabolites with significant changes 1335 compared to the WT, changes in the course of cold acclimation, and with significant 1336 interactions of both effects were selected by 2-way analysis of variance (ANOVA, P < 0.001, 1337 Supplemental Table S1). 1338 1339 1340 Figure 8. Functional enrichment analysis of stress and stimuli related differential gene 1341 expression in reil1-1 reil2-1 at standard cultivation temperature compared to cold 1342 acclimating Col-0 and reil1-1 reil2-1 at 1 day (1 d), 1 week (1 w), or 3 weeks (3 w) after 1343 shift to 10°C. Differential gene expression was determined relative to non-acclimated Col-0 1344 at standard cultivation temperature. Z-scores, P-values and mean log2-fold changes (FC) of 1345 genes belonging to 1940 GO terms were calculated (Zhou et al., 2010; Supplemental Table 1346 S4). 1347 (A) Heat map of mean log2-FC of the top 10 significantly enriched 135 GO terms that 1348

represented responses to stimuli or abiotic and biotic stresses. Ranking was 1349 according to top positive or negative z-score values with mean log2-FC > +0.1 or < -1350 0.1. GO terms are listed with ontology, description, and number of constituting genes. 1351 Bold font of the GO description indicates shared enrichment of the non-acclimated 1352 mutant (0 d) with the acclimating Col-0 at 1 day, 1 week, or 3 weeks. Two general 1353 stimuli- and stress-response GOs as well as the temperature-, cold-, heat-response, 1354



51

water, drought and osmotic stress related GOs were added for comparison. All top 1355 scoring GO were biological processes (P). 1356

(B) Mean log2-FC of GO terms from the non-acclimated mutant (0 d) and acclimating 1357 Col-0 at 1 day, 1 week, 3 weeks (from left to right). All 135 acclimation and response-1358 related GO terms were included. The inserts show the Pearson´s correlation 1359 coefficient (r²) and the slope of a linear regression. The arrows indicate GO:0009631 1360 “cold acclimation”. 1361

1362 1363 Figure 9. Differential expression of genes that were up-regulated in non-acclimated 1364 reil1-1 reil2-1 and significantly changed in 10°C cold acclimating Col-0. 1365

A) Differentially expressed genes (P < 0.01) in non-acclimated reil1-1 reil2-1 that 1366 belonged to GO term GO:0009631 “cold acclimation”. Note that these three genes 1367 were also part of GO:0009409 “response to cold”. 1368

B) Additional differentially expressed genes (P < 0.01 or P < 0.05) that belonged to GO 1369 term GO:0009409 “response to cold”. 1370

C) Selected genes that belonged to GO:0010286 “heat acclimation”. Note that DREB2A 1371 and DREB2B were slightly increased in the non-acclimated mutant and also part of 1372 the long term Col-0 response to a 10°C shift (cf. Figure 8). SKP2B was the only gene 1373 of GO:0010286 “heat acclimation” that was significantly up-regulated at P < 0.01 in 1374 non-acclimated reil1-1 reil2-1. 1375

Relative expression values are log2-transformed fold changes (ratios) compared to non-1376 acclimated Col-0 (mean, +/- standard error). Headers show Arabidopsis gene names and 1377 gene codes in brackets. Significance values of heteroscedastic t-tests comparing non-1378 acclimated mutant to non-acclimated Col-0 are indicated (* 0.01 < P ≤ 0.05, ** P ≤ 0.01). 1379 Circles in the top right corner of each panel indicate that the respective genes were also part 1380 of the water limitation GO terms, GO:0009414 and GO:0009415. 1381

1382

Figure 10. Functional enrichment analysis of ribosome and translation related gene 1383 expression in reil1-1 reil2-1 compared to Col-0 in the non-acclimated state and after 1384 shift to 10°C. 1385

(A) Heat map of mean log2-fold changes (FC) from structural ribosome and translation 1386 related GO terms and selected more specified sub-terms. Reil1-1 reil2-1/Col-0 1387 columns represent mean log2-FCs > +0.1 or < -0.1 of mutant expression ratios 1388 compared to Col-0 in the non-acclimated state (0 d) and at the time points after shift 1389 to 10°C, 1 day (1 d), 1 week (1 w), and 3 weeks (3 w). Log2-FCs with significant 1390 positive or negative enrichment, i.e. z-score values > 2.5 are indicated by *. Columns 1391 reil1-1 reil2-1 and Col-0 at 0 d, 1 d, 1 w, and 3 w represent mean log2-FC of 1392 expression ratios relative to non-acclimated Col-0 (black triangle). Information was 1393 extracted from mean log2-FCs, z-scores, and P-values of a differential gene 1394 expression enrichment analysis covering genes belonging to 1940 GO terms (Zhou 1395 et al., 2010; Supplemental Table S4). 1396

(B) Mean log2-FC (+/- standard error) of cytosolic and chloroplast structural genes as 1397 defined by MapMan/PageMan functional bin annotations (Thimm et al., 2004; Usadel 1398 et al., 2006). Grey columns in each left sub-panel are expression ratios of reil1-1 1399 reil2-1/Col-0 at the given time point. Black and white columns in the right sub-panel 1400 represent the ratios relative to non-acclimated Col-0 (black triangle). 1401

1402 1403 Figure 11. Selected differentially expressed flowering related genes of non-acclimated 1404 (0 d) and 10°C cold acclimating reil1-1 reil2-1 at 1 day (1 d), 1 week (1 w), or 3 weeks (3 1405 w) after shift to 10°C. 1406



52

Relative expression values are mean log2-FC (+/- standard error). Grey columns in each left 1407 sub-panel are expression ratios of reil1-1 reil2-1/Col-0 at the given time points. Black and 1408 white columns in the right sub-panel represent the ratios relative to non-acclimated Col-0 1409 (black triangle). (*, 0.01 < P ≤ 0.05; **, 0,001 < P ≤ 0.01; ***, P ≤ 0.001; heteroscedastic t-1410 tests). 1411 1412 1413 Figure 12. Functional interaction model that summarizes our current insights into the 1414 role of REIL proteins in mature leaves before (20°/18°C, day/ night) and after shift to 1415 low temperature conditions (10°/8°C). 1416 1417 1418

1419



53

Tables 1420

Table 1: Analysis of differentially expressed genes (DEG) of non-acclimated reil1-1 reil2-1 1421

relative to non-acclimated Col-0 WT (0 day) that were also cold responsive transcripts of 1422

Col-0 WT at 1 day, 1 week, or 3 weeks after shift to 10°C relative to non-acclimated Col-0. “1 1423

d, 1 w, or 3 w” lists the sum of genes that were differentially expressed during least at one 1424

time point. “1 d, 1 w, and 3 w” lists the number of genes that were differentially expressed at 1425

all time points. 1426 1427

DEGs at: 0 day 1 day 1 week 3 weeks 1 d, 1 w, 1 d, 1 w, 1428 or 3 w and 3 w 1429 1430

Col-0 1431

all - 3301 2711 3275 6537 594 1432

up - 2726 2323 2682 5310 538 1433

down - 575 388 593 1227 56 1434

reil1-1 reil2-1 number of DEGs that were also 10°C shift responsive in Col-0 1435 1436

count all 428 80 77 100 150 31 1437

up 287 66 67 86 121 31 1438

down 141 14 10 14 29 0 1439

% all 100.0 18.7 18.0 23.4 35.0 7.2 1440

relative up 100.0 23.0 23.3 30.0 42.2 10.8 1441

to 0 day down 100.0 9.9 7.1 9.9 20.6 0.0 1442

1443

Non-acclimated reil1-1 reil2-1 and Col-0 (0 day) were compared by heteroscedastic t-testing 1444 at P < 0.01 (n = 5-6 independent pools of mature rosette leaves from 2-3 plants). 10°C cold 1445 responsive transcripts were selected at P < 0.01 (n = 3 independent pools of mature rosette 1446 leaves from 2-3 plants. The set of 428 DEGs and the subset of 150 genes that were also 1447 10°C shift responsive in Col-0 are reported as supplementary data (Supplemental Table S3). 1448 1449 1450



54

1451



Parsed CitationsAscenzi R, Gantt JS (1999) Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana. Plant MolBiol 41: 159-169

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Barakat A, Szick-Miranda K, Chang IF, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J (2001) The organization of cytoplasmicribosomal protein genes in the Arabidopsis genome. Plant Physiol 127: 398-415


Basu U, Si K, Warner JR, Maitra U (2001) The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is requiredfor 60S ribosomal subunit biogenesis. Mol Cell Biol 21: 1453-1462


Bent, AF (2000) Arabidopsis in planta transformation. Uses, mechanisms, and prospects for transformation of other species. PlantPhysiology 124: 1540-1547


Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis ofArabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510


Browning KS, Bailey-Serres J (2015) Mechanism of cytoplasmic mRNA translation. Arabidopsis Book 13: e0176Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Burks EA, Bezerra PP, Le H, Gallie DR, Browning KS (2001) Plant initiation factor 3 subunit composition resembles mammalianinitiation factor 3 and has a novel subunit. J Biol Chem 276: 2122-2131


Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14: 512–519Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Calderón-Villalobos LIA, Nill C, Marrocco K, Kretsch T, Schwechheimer C (2007) The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress. Gene 392: 106-116


Chang IF, Szick-Miranda K, Pan S, Bailey-Serres J (2005) Proteomic characterization of evolutionarily conserved and variable proteinsof Arabidopsis cytosolic ribosomes. Plant Physiol 137: 848-862


Chen MK, Hsu WH, Lee PF, Thiruvengadam M, Chen HL, Yang CH (2011) The MADS box gene, FOREVER YOUNG FLOWER, acts as arepressor controlling floral organ senescence and abscission in Arabidopsis. Plant J 68: 168-185


Creff A, Sormani R, Desnos T (2010) The two Arabidopsis RPS6 genes, encoding for cytoplasmic ribosomal proteins S6, arefunctionally equivalent. Plant Molecular Biology 73: 533–546


Degenhardt RF, Bonham-Smith PC (2008) Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to thenucleolus and are disparately required for normal development. Plant Physiol 147: 128–142


http://www.ncbi.nlm.nih.gov/pubmed?term=Ascenzi R%2C Gantt JS %281999%29 Molecular genetic analysis of the drought%2Dinducible linker histone variant in Arabidopsis thaliana%2E Plant Mol Biol 41%3A 159%2D169&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ascenzi R, Gantt JS (1999) Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana. Plant Mol Biol 41: 159-169

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ascenzi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ascenzi&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Barakat A%2C Szick%2DMiranda K%2C Chang IF%2C Guyot R%2C Blanc G%2C Cooke R%2C Delseny M%2C Bailey%2DSerres J %282001%29 The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome%2E Plant Physiol 127%3A 398%2D415&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Barakat A, Szick-Miranda K, Chang IF, Guyot R, Blanc G, Cooke R, Delseny M, Bailey-Serres J (2001) The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol 127: 398-415

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Barakat&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Barakat&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Basu U%2C Si K%2C Warner JR%2C Maitra U %282001%29 The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis%2E Mol Cell Biol 21%3A 1453%2D1462&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Basu U, Si K, Warner JR, Maitra U (2001) The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol Cell Biol 21: 1453-1462

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Basu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Basu&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bent%2C AF %282000%29 Arabidopsis in planta transformation%2E Uses%2C mechanisms%2C and prospects for transformation of other species%2E Plant Physiology 124%3A 1540%2D1547&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bent, AF (2000) Arabidopsis in planta transformation. Uses, mechanisms, and prospects for transformation of other species. Plant Physiology 124: 1540-1547

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bent,&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis in planta transformation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis in planta transformation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bent,&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Boyes DC%2C Zayed AM%2C Ascenzi R%2C McCaskill AJ%2C Hoffman NE%2C Davis KR%2C G�rlach J %282001%29 Growth stage%2Dbased phenotypic analysis of Arabidopsis%3A A model for high throughput functional genomics in plants%2E Plant Cell 13%3A 1499%2D1510&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, G�rlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Boyes&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Boyes&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Browning KS%2C Bailey%2DSerres J %282015%29 Mechanism of cytoplasmic mRNA translation%2E Arabidopsis Book 13%3A e0176&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Browning KS, Bailey-Serres J (2015) Mechanism of cytoplasmic mRNA translation. Arabidopsis Book 13: e0176

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Browning&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mechanism of cytoplasmic mRNA translation.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mechanism of cytoplasmic mRNA translation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Browning&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Burks EA%2C Bezerra PP%2C Le H%2C Gallie DR%2C Browning KS %282001%29 Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit%2E J Biol Chem 276%3A 2122%2D2131&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Burks EA, Bezerra PP, Le H, Gallie DR, Browning KS (2001) Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit. J Biol Chem 276: 2122-2131

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Burks&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Burks&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Byrne ME %282009%29 A role for the ribosome in development%2E Trends Plant Sci 14%3A 512�??519&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Byrne ME (2009) A role for the ribosome in development. Trends Plant Sci 14: 512?519

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Byrne&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A role for the ribosome in development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A role for the ribosome in development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Byrne&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Calder�n%2DVillalobos LIA%2C Nill C%2C Marrocco K%2C Kretsch T%2C Schwechheimer C %282007%29 The evolutionarily conserved Arabidopsis thaliana F%2Dbox protein AtFBP7 is required for efficient translation during temperature stress%2E Gene 392%3A 106%2D116&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Calder�n-Villalobos LIA, Nill C, Marrocco K, Kretsch T, Schwechheimer C (2007) The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress. Gene 392: 106-116

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Calderón-Villalobos&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Calderón-Villalobos&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chang IF%2C Szick%2DMiranda K%2C Pan S%2C Bailey%2DSerres J %282005%29 Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes%2E Plant Physiol 137%3A 848%2D862&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chang IF, Szick-Miranda K, Pan S, Bailey-Serres J (2005) Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes. Plant Physiol 137: 848-862

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Chang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chang&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Chen MK%2C Hsu WH%2C Lee PF%2C Thiruvengadam M%2C Chen HL%2C Yang CH %282011%29 The MADS box gene%2C FOREVER YOUNG FLOWER%2C acts as a repressor controlling floral organ senescence and abscission in Arabidopsis%2E Plant J 68%3A 168%2D185&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Chen MK, Hsu WH, Lee PF, Thiruvengadam M, Chen HL, Yang CH (2011) The MADS box gene, FOREVER YOUNG FLOWER, acts as a repressor controlling floral organ senescence and abscission in Arabidopsis. Plant J 68: 168-185

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Chen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The MADS box gene, FOREVER YOUNG FLOWER, acts as a repressor controlling floral organ senescence and abscission in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The MADS box gene, FOREVER YOUNG FLOWER, acts as a repressor controlling floral organ senescence and abscission in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Creff A%2C Sormani R%2C Desnos T %282010%29 The two Arabidopsis RPS6 genes%2C encoding for cytoplasmic ribosomal proteins S6%2C are functionally equivalent%2E Plant Molecular Biology 73%3A 533�??546&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Creff A, Sormani R, Desnos T (2010) The two Arabidopsis RPS6 genes, encoding for cytoplasmic ribosomal proteins S6, are functionally equivalent. Plant Molecular Biology 73: 533?546

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Creff&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The two Arabidopsis RPS6 genes, encoding for cytoplasmic ribosomal proteins S6, are functionally equivalent.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The two Arabidopsis RPS6 genes, encoding for cytoplasmic ribosomal proteins S6, are functionally equivalent.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Creff&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1



del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2pathway in response to light. Plant Cell 14: 3057–3071


Demoinet E, Jacquier A, Lutfalla G, Fromont-Racine M (2007) The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmicrecycling of preribosomal factors in Saccharomyces cerevisiae. RNA 13: 1570-1581


Dethloff F, Erban A, Orf I, Alpers J, Fehrle I, Beine-Golovchuk O, Schmidt S, Schwachtje J, Kopka J (2014) Profiling methods to identifycold-regulated primary metabolites using gas chromatography coupled to mass spectrometry. In: Hincha DK, Zuther E (eds) Plant coldacclimation: Methods and Protocols. Methods Mol Biol 1166: 171-197


Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucl Acids Res 38: W64-W70Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functionalgenomics and proteomics. Plant J 45: 616-629


Giavalisco P, Wilson D, Kreitler T, Lehrach H, Klose J, Gobom J, Fucini P (2005) High heterogeneity within the ribosomal proteins ofthe Arabidopsis thaliana 80S ribosome. Plant Mol Biol 57: 577-591.


Greber BJ, Boehringer D, Montellese C, Ban N (2012) Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the60S ribosomal subunit. Nature Struct Mol Biol 19: 1228-1234


Greber BJ, Gerhardy S, Leitner A, Leibundgut M, Salem M, Boehringer D, Leulliot N, Aebersold R, Panse VG, Ban N (2016) Insertion ofthe biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation. Cell 164: 91-102


Grefen C, Obrdlik P, Harter K (2009) The determination of protein–protein Interactions by the mating-based split-ubiquitin system(mbSUS). Methods Mol Biol 479: 217-233


Grefen C, Donald N, Schumacher K, Blatt MR (2010) A Ubiquitin-10 promoter-based vector set for fluorescent protein taggingfacilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J 64: 355-365


Guo Y, Xiong L, Ishitani M, Zhu JK (2002) An Arabidopsis mutation in translation elongation factor 2 causes superinduction ofCBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc Nat AcadSci 99: 7786-7791


Guy CL, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132: 220-235Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=Degenhardt RF%2C Bonham%2DSmith PC %282008%29 Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development%2E Plant Physiol 147%3A 128�??142&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Degenhardt RF, Bonham-Smith PC (2008) Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol 147: 128?142

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Degenhardt&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Degenhardt&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=del Pozo JC%2C Boniotti MB%2C Gutierrez C %282002%29 Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin%2DSCFAtSKP2 pathway in response to light%2E Plant Cell 14%3A 3057�??3071&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. Plant Cell 14: 3057?3071

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=del&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=del&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Demoinet E%2C Jacquier A%2C Lutfalla G%2C Fromont%2DRacine M %282007%29 The Hsp40 chaperone Jjj1 is required for the nucleo%2Dcytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae%2E RNA 13%3A 1570%2D1581&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Demoinet E, Jacquier A, Lutfalla G, Fromont-Racine M (2007) The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 13: 1570-1581

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Demoinet&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Demoinet&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dethloff F%2C Erban A%2C Orf I%2C Alpers J%2C Fehrle I%2C Beine%2DGolovchuk O%2C Schmidt S%2C Schwachtje J%2C Kopka J %282014%29 Profiling methods to identify cold%2Dregulated primary metabolites using gas chromatography coupled to mass spectrometry%2E In%3A Hincha DK%2C Zuther E %28eds%29 Plant cold acclimation%3A Methods and Protocols%2E Methods Mol Biol 1166%3A 171%2D197&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dethloff F, Erban A, Orf I, Alpers J, Fehrle I, Beine-Golovchuk O, Schmidt S, Schwachtje J, Kopka J (2014) Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry. In: Hincha DK, Zuther E (eds) Plant cold acclimation: Methods and Protocols. Methods Mol Biol 1166: 171-197

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Dethloff&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dethloff&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Du Z%2C Zhou X%2C Ling Y%2C Zhang Z%2C Su Z %282010%29 AgriGO%3A a GO analysis toolkit for the agricultural community%2E Nucl Acids Res 38%3A W64%2DW70&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucl Acids Res 38: W64-W70

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Du&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=AgriGO: a GO analysis toolkit for the agricultural community&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=AgriGO: a GO analysis toolkit for the agricultural community&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Du&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Earley KW%2C Haag JR%2C Pontes O%2C Opper K%2C Juehne T%2C Song K%2C Pikaard CS %282006%29 Gateway%2Dcompatible vectors for plant functional genomics and proteomics%2E Plant J 45%3A 616%2D629&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Earley&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Gateway-compatible vectors for plant functional genomics and proteomics&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Gateway-compatible vectors for plant functional genomics and proteomics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Earley&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Giavalisco P%2C Wilson D%2C Kreitler T%2C Lehrach H%2C Klose J%2C Gobom J%2C Fucini P %282005%29 High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome%2E Plant Mol Biol 57%3A 577%2D591%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Giavalisco P, Wilson D, Kreitler T, Lehrach H, Klose J, Gobom J, Fucini P (2005) High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol Biol 57: 577-591.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Giavalisco&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Giavalisco&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Greber BJ%2C Boehringer D%2C Montellese C%2C Ban N %282012%29 Cryo%2DEM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit%2E Nature Struct Mol Biol 19%3A 1228%2D1234&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Greber BJ, Boehringer D, Montellese C, Ban N (2012) Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nature Struct Mol Biol 19: 1228-1234

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Greber&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Greber&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Greber BJ%2C Gerhardy S%2C Leitner A%2C Leibundgut M%2C Salem M%2C Boehringer D%2C Leulliot N%2C Aebersold R%2C Panse VG%2C Ban N %282016%29 Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation%2E Cell 164%3A 91%2D102&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Greber BJ, Gerhardy S, Leitner A, Leibundgut M, Salem M, Boehringer D, Leulliot N, Aebersold R, Panse VG, Ban N (2016) Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation. Cell 164: 91-102

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Greber&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Greber&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grefen C%2C Obrdlik P%2C Harter K %282009%29 The determination of protein�??protein Interactions by the mating%2Dbased split%2Dubiquitin system %28mbSUS%29%2E Methods Mol Biol 479%3A 217%2D233&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Grefen C, Obrdlik P, Harter K (2009) The determination of protein?protein Interactions by the mating-based split-ubiquitin system (mbSUS). Methods Mol Biol 479: 217-233

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grefen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The determination of proteinâ�?�?protein Interactions by the mating-based split-ubiquitin system (mbSUS)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The determination of proteinâ�?�?protein Interactions by the mating-based split-ubiquitin system (mbSUS)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grefen&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Grefen C%2C Donald N%2C Schumacher K%2C Blatt MR %282010%29 A Ubiquitin%2D10 promoter%2Dbased vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies%2E Plant J 64%3A 355%2D365&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Grefen C, Donald N, Schumacher K, Blatt MR (2010) A Ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J 64: 355-365

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Grefen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A Ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A Ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Grefen&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guo Y%2C Xiong L%2C Ishitani M%2C Zhu JK %282002%29 An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF%2FDREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures%2E Proc Nat Acad Sci 99%3A 7786%2D7791&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Guo Y, Xiong L, Ishitani M, Zhu JK (2002) An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc Nat Acad Sci 99: 7786-7791

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Guo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guo&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Guy CL%2C Kaplan F%2C Kopka J%2C Selbig J%2C Hincha DK %282008%29 Metabolomics of temperature stress%2E Physiol Plant 132%3A 220%2D235&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Guy CL, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132: 220-235

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Guy&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Metabolomics of temperature stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Metabolomics of temperature stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guy&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1


Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoSGenetics 1: e26


Horiguchi G, Van Lijsebettens M, Candelae H, Micole JL, Tsukaya H (2012) Ribosomes and translation in plant developmental control.Plant Sci 191: 24-34


Hummel J, Strehmel N, Selbig J, Walther D, Kopka J (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics 6: 322-333


Hung NJ, Johnson AW (2006) Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 inSaccharomyces cerevisiae. Mol Cell Biol 26: 3718-3727


Iwase M, Toh-e A (2004) Ybr267w is a new cytoplasmic protein belonging to the mitotic signalling network of Saccharomycescerevisiae. Cell Struct Funct 29: 1-15


Johnson AW, Lund E, Dahlberg J (2002) Nuclear export of ribosomal subunits. Trends Biochem Sci 27: 580-585Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kang MJ, Jin HS, Noh YS, Noh B (2015) Repression of flowering under a non-inductive photoperiod by the HDA9-AGL19-FT module inArabidopsis. New Phytologist 206: 281-294


Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolomeof Arabidopsis. Plant Physiol 136: 4159-4168


Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation ofArabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967-981


Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stressand dehydration stress conditions in Arabidopsis thaliana. Plant J 38: 823-839


Kim GT, Tsukaya H, Uchimiya H (1998) The CURLY LEAF gene controls both division and elongation of cells during the expansion ofthe leaf blade in Arabidopsis thaliana. Planta 206: 175-183


Kim W, Latrasse D, Servet C, Zhou DX (2013) Arabidopsis histone deacetylase HDA9 regulates flowering time through repression ofAGL19. Biochem Biophys Res Commun 432: 394-398


Klinge S, Voigts-Hoffmann F, Leibundgut M, Arpagaus S, Ban N (2011) Crystal structure of the eukaryotic 60S ribosomal subunit incomplex with initiation factor 6. Science 334: 941-948

Pubmed: Author and Title www.plantphysiol.orgon September 9, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Hannah MA%2C Heyer AG%2C Hincha DK %282005%29 A global survey of gene regulation during cold acclimation in Arabidopsis thaliana%2E PLoS Genetics 1%3A e26&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genetics 1: e26

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hannah&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A global survey of gene regulation during cold acclimation in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A global survey of gene regulation during cold acclimation in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hannah&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Horiguchi G%2C Van Lijsebettens M%2C Candelae H%2C Micole JL%2C Tsukaya H %282012%29 Ribosomes and translation in plant developmental control%2E Plant Sci 191%3A 24%2D34&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Horiguchi G, Van Lijsebettens M, Candelae H, Micole JL, Tsukaya H (2012) Ribosomes and translation in plant developmental control. Plant Sci 191: 24-34

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Horiguchi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Ribosomes and translation in plant developmental control&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Ribosomes and translation in plant developmental control&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Horiguchi&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hummel J%2C Strehmel N%2C Selbig J%2C Walther D%2C Kopka J %282010%29 Decision tree supported substructure prediction of metabolites from GC%2DMS profiles%2E Metabolomics 6%3A 322%2D333&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hummel J, Strehmel N, Selbig J, Walther D, Kopka J (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics 6: 322-333

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hummel&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Decision tree supported substructure prediction of metabolites from GC-MS profiles&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Decision tree supported substructure prediction of metabolites from GC-MS profiles&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hummel&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hung NJ%2C Johnson AW %282006%29 Nuclear recycling of the pre%2D60S ribosomal subunit%2Dassociated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae%2E Mol Cell Biol 26%3A 3718%2D3727&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hung NJ, Johnson AW (2006) Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae. Mol Cell Biol 26: 3718-3727

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hung&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hung&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Iwase M%2C Toh%2De A %282004%29 Ybr267w is a new cytoplasmic protein belonging to the mitotic signalling network of Saccharomyces cerevisiae%2E Cell Struct Funct 29%3A 1%2D15&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Iwase M, Toh-e A (2004) Ybr267w is a new cytoplasmic protein belonging to the mitotic signalling network of Saccharomyces cerevisiae. Cell Struct Funct 29: 1-15

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Iwase&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Ybr267w is a new cytoplasmic protein belonging to the mitotic signalling network of Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Ybr267w is a new cytoplasmic protein belonging to the mitotic signalling network of Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Iwase&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Johnson AW%2C Lund E%2C Dahlberg J %282002%29 Nuclear export of ribosomal subunits%2E Trends Biochem Sci 27%3A 580%2D585&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Johnson AW, Lund E, Dahlberg J (2002) Nuclear export of ribosomal subunits. Trends Biochem Sci 27: 580-585

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Johnson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Nuclear export of ribosomal subunits&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Nuclear export of ribosomal subunits&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Johnson&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kang MJ%2C Jin HS%2C Noh YS%2C Noh B %282015%29 Repression of flowering under a non%2Dinductive photoperiod by the HDA9%2DAGL19%2DFT module in Arabidopsis%2E New Phytologist 206%3A 281%2D294&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kang MJ, Jin HS, Noh YS, Noh B (2015) Repression of flowering under a non-inductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis. New Phytologist 206: 281-294

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Repression of flowering under a non-inductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Repression of flowering under a non-inductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kaplan F%2C Kopka J%2C Haskell DW%2C Zhao W%2C Schiller KC%2C Gatzke N%2C Sung DY%2C Guy CL %282004%29 Exploring the temperature%2Dstress metabolome of Arabidopsis%2E Plant Physiol 136%3A 4159%2D4168&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136: 4159-4168

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kaplan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Exploring the temperature-stress metabolome of Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Exploring the temperature-stress metabolome of Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kaplan&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kaplan F%2C Kopka J%2C Sung DY%2C Zhao W%2C Popp M%2C Porat R%2C Guy CL %282007%29 Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold%2Dregulated gene expression with modifications in metabolite content%2E Plant J 50%3A 967%2D981&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50: 967-981

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kaplan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kaplan&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kawaguchi R%2C Girke T%2C Bray EA%2C Bailey%2DSerres J %282004%29 Differential mRNA translation contributes to gene regulation under non%2Dstress and dehydration stress conditions in Arabidopsis thaliana%2E Plant J 38%3A 823%2D839&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 38: 823-839

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kawaguchi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kawaguchi&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim GT%2C Tsukaya H%2C Uchimiya H %281998%29 The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana%2E Planta 206%3A 175%2D183&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim GT, Tsukaya H, Uchimiya H (1998) The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana. Planta 206: 175-183

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kim&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The CURLY LEAF gene controls both division and elongation of cells during the expansion of the leaf blade in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=1998&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim W%2C Latrasse D%2C Servet C%2C Zhou DX %282013%29 Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19%2E Biochem Biophys Res Commun 432%3A 394%2D398&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim W, Latrasse D, Servet C, Zhou DX (2013) Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem Biophys Res Commun 432: 394-398

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kim&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Klinge S%2C Voigts%2DHoffmann F%2C Leibundgut M%2C Arpagaus S%2C Ban N %282011%29 Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6%2E Science 334%3A 941%2D948&dopt=abstract


CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Kobayashi Y, Weigel D (2007) Move on up, it’s time for change - mobile signals controlling photoperiod-dependent flowering. GenesDev 21: 2371-2384


Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmueller E, Doermann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L,Fernie AR, Steinhauser D (2005) [email protected]: the Golm Metabolome Database. Bioinformatics 21: 1635-1638


Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62: 4731–4748Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lebreton A, Saveanu C, Decourty L, Rain JC, Jacquier A, Fromont-Racine M (2006) A functional network involved in the recycling ofnucleocytoplasmic pre-60S factors. J Cell Biol 173: 349-360


Lee J, Yun JY, Zhao W, Shen WH, Amasino RM (2015) A methyltransferase required for proper timing of the vernalization response inArabidopsis. Proc Nat Acad Sci 112: 2269-2274


Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates floweringsignals in Arabidopsis. Development 135: 1481-1491


Lo KY, Li ZH, Bussiere C, Bresson S, Marcotte EM, Johnson AW (2010) Defining the pathway of cytoplasmic maturation of the 60Sribosomal subunit. Mol Cell 39: 196-208


Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography - massspectrometry (GC-MS) based metabolite profiling experiments. Bioinformatics 24: 732-737


Ma C, Wu S, Li N, Chen Y, Yan K, Li Z, Zheng L, Lei J, Woolford Jr JL, Gao N (2017) Structural snapshot of cytoplasmic pre-60Sribosomal particles bound by Nmd3, Lsg1, Tif6 and Reh1. Nat Struct Mol Biol 24: 214-220


Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, SuzukiH, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified byintegrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150: 1972-1980


Meyer AE, Hung NJ, Yang PZ, Johnson AW, Craig EA (2007) The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunitbiogenesis. Proc Natl Acad Sci USA 104: 1558-1563


Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15: 473-497


Mustroph A, Juntawong P, Bailey-Serres J (2009) Isolation of plant polysomal mRNA by differential centrifugation and ribosome www.plantphysiol.orgon September 9, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://search.crossref.org/?page=1&rows=2&q=Klinge S, Voigts-Hoffmann F, Leibundgut M, Arpagaus S, Ban N (2011) Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 334: 941-948

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Klinge&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klinge&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kobayashi Y%2C Weigel D %282007%29 Move on up%2C it�??s time for change %2D mobile signals controlling photoperiod%2Ddependent flowering%2E Genes Dev 21%3A 2371%2D2384&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kobayashi Y, Weigel D (2007) Move on up, it?s time for change - mobile signals controlling photoperiod-dependent flowering. Genes Dev 21: 2371-2384

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kobayashi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Move on up, itâ�?�?s time for change - mobile signals controlling photoperiod-dependent flowering&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Move on up, itâ�?�?s time for change - mobile signals controlling photoperiod-dependent flowering&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kobayashi&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kopka J%2C Schauer N%2C Krueger S%2C Birkemeyer C%2C Usadel B%2C Bergmueller E%2C Doermann P%2C Weckwerth W%2C Gibon Y%2C Stitt M%2C Willmitzer L%2C Fernie AR%2C Steinhauser D %282005%29 GMD%40CSB%2EDB%3A the Golm Metabolome Database%2E Bioinformatics 21%3A 1635%2D1638&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmueller E, Doermann P, Weckwerth W, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D (2005) [email protected]: the Golm Metabolome Database. Bioinformatics 21: 1635-1638

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kopka&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=GMD@CSB&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=GMD@CSB&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kopka&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lata C%2C Prasad M %282011%29 Role of DREBs in regulation of abiotic stress responses in plants%2E J Exp Bot 62%3A 4731�??4748&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62: 4731?4748

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lata&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Role of DREBs in regulation of abiotic stress responses in plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Role of DREBs in regulation of abiotic stress responses in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lata&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lebreton A%2C Saveanu C%2C Decourty L%2C Rain JC%2C Jacquier A%2C Fromont%2DRacine M %282006%29 A functional network involved in the recycling of nucleocytoplasmic pre%2D60S factors%2E J Cell Biol 173%3A 349%2D360&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lebreton A, Saveanu C, Decourty L, Rain JC, Jacquier A, Fromont-Racine M (2006) A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J Cell Biol 173: 349-360

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lebreton&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A functional network involved in the recycling of nucleocytoplasmic pre-60S factors&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A functional network involved in the recycling of nucleocytoplasmic pre-60S factors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lebreton&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lee J%2C Yun JY%2C Zhao W%2C Shen WH%2C Amasino RM %282015%29 A methyltransferase required for proper timing of the vernalization response in Arabidopsis%2E Proc Nat Acad Sci 112%3A 2269%2D2274&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lee J, Yun JY, Zhao W, Shen WH, Amasino RM (2015) A methyltransferase required for proper timing of the vernalization response in Arabidopsis. Proc Nat Acad Sci 112: 2269-2274

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lee&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A methyltransferase required for proper timing of the vernalization response in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A methyltransferase required for proper timing of the vernalization response in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lee&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Liu C%2C Chen H%2C Er HL%2C Soo HM%2C Kumar PP%2C Han JH%2C Liou YC%2C Yu H %282008%29 Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis%2E Development 135%3A 1481%2D1491&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Liu C, Chen H, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135: 1481-1491

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Liu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Liu&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lo KY%2C Li ZH%2C Bussiere C%2C Bresson S%2C Marcotte EM%2C Johnson AW %282010%29 Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit%2E Mol Cell 39%3A 196%2D208&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lo KY, Li ZH, Bussiere C, Bresson S, Marcotte EM, Johnson AW (2010) Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol Cell 39: 196-208

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lo&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Luedemann A%2C Strassburg K%2C Erban A%2C Kopka J %282008%29 TagFinder for the quantitative analysis of gas chromatography %2D mass spectrometry %28GC%2DMS%29 based metabolite profiling experiments%2E Bioinformatics 24%3A 732%2D737&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography - mass spectrometry (GC-MS) based metabolite profiling experiments. Bioinformatics 24: 732-737

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Luedemann&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=TagFinder for the quantitative analysis of gas chromatography - mass spectrometry (GC-MS) based metabolite profiling experiments&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=TagFinder for the quantitative analysis of gas chromatography - mass spectrometry (GC-MS) based metabolite profiling experiments&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Luedemann&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ma C%2C Wu S%2C Li N%2C Chen Y%2C Yan K%2C Li Z%2C Zheng L%2C Lei J%2C Woolford Jr JL%2C Gao N %282017%29 Structural snapshot of cytoplasmic pre%2D60S ribosomal particles bound by Nmd3%2C Lsg1%2C Tif6 and Reh1%2E Nat Struct Mol Biol 24%3A 214%2D220&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ma C, Wu S, Li N, Chen Y, Yan K, Li Z, Zheng L, Lei J, Woolford Jr JL, Gao N (2017) Structural snapshot of cytoplasmic pre-60S ribosomal particles bound by Nmd3, Lsg1, Tif6 and Reh1. Nat Struct Mol Biol 24: 214-220

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ma&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ma&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Maruyama K%2C Takeda M%2C Kidokoro S%2C Yamada K%2C Sakuma Y%2C Urano K%2C Fujita M%2C Yoshiwara K%2C Matsukura S%2C Morishita Y%2C Sasaki R%2C Suzuki H%2C Saito K%2C Shibata D%2C Shinozaki K%2C Yamaguchi%2DShinozaki K %282009%29 Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A%2E Plant Physiol 150%3A 1972%2D1980&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, Suzuki H, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150: 1972-1980

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Maruyama&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Maruyama&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Meyer AE%2C Hung NJ%2C Yang PZ%2C Johnson AW%2C Craig EA %282007%29 The specialized cytosolic J%2Dprotein%2C Jjj1%2C functions in 60S ribosomal subunit biogenesis%2E Proc Natl Acad Sci USA 104%3A 1558%2D1563&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Meyer AE, Hung NJ, Yang PZ, Johnson AW, Craig EA (2007) The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc Natl Acad Sci USA 104: 1558-1563

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Meyer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Meyer&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Murashige T%2C Skoog F %281962%29 A revised medium for rapid growth and bio assays with tobacco tissue cultures%2E Physiol Plantarum 15%3A 473%2D497&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15: 473-497

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Murashige&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A revised medium for rapid growth and bio assays with tobacco tissue cultures&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A revised medium for rapid growth and bio assays with tobacco tissue cultures&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Murashige&as_ylo=1962&as_allsubj=all&hl=en&c2coff=1


immunopurification methods. Methods Mol Biol 553: 109-126Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Nishimura K, Ashida H, Ogawa T, Yokota A (2010) A DEAD box protein is required for formation of a hidden break in Arabidopsischloroplast 23S rRNA. Plant J 63: 766-777


Ó’Maoiléidigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwaśniewska K, Das P, Lohan AJ, Loftus B, Graciet E, Wellmer F (2013)Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 25: 2482-2503


Palm D, Simm S, Darm K, Weis BL, Ruprecht M, Schleiff E, Scharf C (2016) Proteome distribution between nucleoplasm and nucleolusand its relation to ribosome biogenesis in Arabidopsis thaliana. RNA Biol 13: 441-454


Panse VG, Johnson AW (2010) Maturation of eukaryotic ribosomes: Acquisition of functionality. Trends Biochem Sci 35: 260-266Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Parnell KM, Bass BL (2009) Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation. Mol CellBiol 29: 4014-4023


Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JWS, Shaw PJ (2005) Proteomicanalysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16: 260–269


Piques M, Schulze WX, Höhne M, Usadel B, Gibon Y, Rohwer J, Stitt M (2009) Ribosome and transcript copy numbers, polysomeoccupancy and enzyme dynamics in Arabidopsis. Mol Syst Biol 5: 314.


Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gaschromatography-mass spectrometry. Plant J 23: 131-142


Rohde P, Hincha DK, Heyer AG (2004) Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions(Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J 38: 790-799


Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs throughtranslational regulation of auxin response factors. Proc Natl Acad Sci USA 109: 19537-19544


Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat)for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247-259


Salvo-Chirnside E, Kane S, Kerr LE (2011) Protocol: high throughput silica-based purification of RNA from Arabidopsis seedlings in a96-well format. Plant Methods 7: 40

Pubmed: Author and TitleCrossRef: Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=Mustroph A%2C Juntawong P%2C Bailey%2DSerres J %282009%29 Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods%2E Methods Mol Biol 553%3A 109%2D126&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mustroph A, Juntawong P, Bailey-Serres J (2009) Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol Biol 553: 109-126

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mustroph&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mustroph&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nishimura K%2C Ashida H%2C Ogawa T%2C Yokota A %282010%29 A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA%2E Plant J 63%3A 766%2D777&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nishimura K, Ashida H, Ogawa T, Yokota A (2010) A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA. Plant J 63: 766-777

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nishimura&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nishimura&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=�?�??Maoiléidigh DS%2C Wuest SE%2C Rae L%2C Raganelli A%2C Ryan PT%2C Kwa�?niewska K%2C Das P%2C Lohan AJ%2C Loftus B%2C Graciet E%2C Wellmer F %282013%29 Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS%2E Plant Cell 25%3A 2482%2D2503&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=�?Maoil�idigh DS, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwa?niewska K, Das P, Lohan AJ, Loftus B, Graciet E, Wellmer F (2013) Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 25: 2482-2503

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=�?�?â�?�?Maoil�?©idigh&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=�?�?â�?�?Maoil�?©idigh&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Palm D%2C Simm S%2C Darm K%2C Weis BL%2C Ruprecht M%2C Schleiff E%2C Scharf C %282016%29 Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana%2E RNA Biol 13%3A 441%2D454&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Palm D, Simm S, Darm K, Weis BL, Ruprecht M, Schleiff E, Scharf C (2016) Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana. RNA Biol 13: 441-454

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Palm&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Palm&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Panse VG%2C Johnson AW %282010%29 Maturation of eukaryotic ribosomes%3A Acquisition of functionality%2E Trends Biochem Sci 35%3A 260%2D266&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Panse VG, Johnson AW (2010) Maturation of eukaryotic ribosomes: Acquisition of functionality. Trends Biochem Sci 35: 260-266

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Panse&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Maturation of eukaryotic ribosomes: Acquisition of functionality&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Maturation of eukaryotic ribosomes: Acquisition of functionality&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Panse&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parnell KM%2C Bass BL %282009%29 Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation%2E Mol Cell Biol 29%3A 4014%2D4023&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Parnell KM, Bass BL (2009) Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation. Mol Cell Biol 29: 4014-4023

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Parnell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Parnell&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pendle AF%2C Clark GP%2C Boon R%2C Lewandowska D%2C Lam YW%2C Andersen J%2C Mann M%2C Lamond AI%2C Brown JWS%2C Shaw PJ %282005%29 Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions%2E Mol Biol Cell 16%3A 260�??269&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JWS, Shaw PJ (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16: 260?269

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pendle&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pendle&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Piques M%2C Schulze WX%2C H�hne M%2C Usadel B%2C Gibon Y%2C Rohwer J%2C Stitt M %282009%29 Ribosome and transcript copy numbers%2C polysome occupancy and enzyme dynamics in Arabidopsis%2E Mol Syst Biol 5%3A 314%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Piques M, Schulze WX, H�hne M, Usadel B, Gibon Y, Rohwer J, Stitt M (2009) Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol Syst Biol 5: 314.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Piques&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Piques&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Roessner U%2C Wagner C%2C Kopka J%2C Trethewey RN%2C Willmitzer L %282000%29 Simultaneous analysis of metabolites in potato tuber by gas chromatography%2Dmass spectrometry%2E Plant J 23%3A 131%2D142&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J 23: 131-142

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Roessner&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Roessner&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rohde P%2C Hincha DK%2C Heyer AG %282004%29 Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions %28Columbia%2D0 and C24%29 that show differences in non%2Dacclimated and acclimated freezing tolerance%2E Plant J 38%3A 790%2D799&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rohde P, Hincha DK, Heyer AG (2004) Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J 38: 790-799

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rohde&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rohde&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rosado A%2C Li R%2C van de Ven W%2C Hsu E%2C Raikhel NV %282012%29 Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors%2E Proc Natl Acad Sci USA 109%3A 19537%2D19544&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci USA 109: 19537-19544

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rosado&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rosado&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Rosso MG%2C Li Y%2C Strizhov N%2C Reiss B%2C Dekker K%2C Weisshaar B %282003%29 An Arabidopsis thaliana T%2DDNA mutagenized population %28GABI%2DKat%29 for flanking sequence tag%2Dbased reverse genetics%2E Plant Mol Biol 53%3A 247%2D259&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247-259

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rosso&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Rosso&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Salvo%2DChirnside E%2C Kane S%2C Kerr LE %282011%29 Protocol%3A high throughput silica%2Dbased purification of RNA from Arabidopsis seedlings in a 96%2Dwell format%2E Plant Methods 7%3A 40&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Salvo-Chirnside E, Kane S, Kerr LE (2011) Protocol: high throughput silica-based purification of RNA from Arabidopsis seedlings in a 96-well format. Plant Methods 7: 40


Google Scholar: Author Only Title Only Author and Title

Schmidt S, Dethloff F, Beine-Golovchuk O, Kopka J (2013) The REIL1 and REIL2 proteins of Arabidopsis thaliana are required for leafgrowth in the cold. Plant Physiol 163: 1623-1639


Schmidt S, Dethloff F, Beine-Golovchuk O, Kopka J (2014) REIL proteins of Arabidopsis thaliana interact in yeast-2-hybrid assays withhomologs of the yeast Rlp24, Rpl24A, Rlp24B, Arx1 and Jjj1 proteins. Plant Signal Behav 9: e28224


Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124: 1477-1480Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Schönrock N, Bouveret R, Leroy O, Borghi L, Köhler C, Gruissem W, Hennig L (2006) Polycomb-group proteins repress the floralactivator AGL19 in the FLC-independent vernalization pathway. Genes Development 20: 1667-1678


Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2015) Natural variation in flavonol and anthocyanin metabolism during coldacclimation in Arabidopsis thaliana accessions. Plant Cell Environ 38: 1658-1672


Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2016) Flavonoids are determinants of freezing tolerance and cold acclimation inArabidopsis thaliana accessions. Sci Rep 6: 34027


Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses.Curr Opin Plant Biol 6: 410-417


Song J, Angel A, Howard M, Dean C (2012) Vernalization – a cold-induced epigenetic switch. J Cell Sci 125: 1-9Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sormani R, Masclaux-Daubresse C, Daniele-Vedele F, Chardon F (2011) Transcriptional regulation of ribosome components aredetermined by stress according to cellular compartments in Arabidopsis thaliana. PLoS ONE 6: e28070


Strassburg K, Walther D, Takahashi H, Kanaya S, Kopka J (2010) Dynamic transcriptional and metabolic responses in yeast adapting totemperature stress. OMICS J Integr Biol 14: 249-259


Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013) R-Loop stabilization represses antisense transcription at theArabidopsis FLC locus. Science 340: 619-621


Thalhammer A, Hincha DK, Zuther E (2014) Measuring Freezing Tolerance: Electrolyte Leakage and Chlorophyll Fluorescence Assays.In: Hincha DK, Zuther E (eds) Plant cold acclimation: Methods and Protocols. Methods Mol Biol 1166: 15-24


Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Miñambres M, Walther D, Schulze WX, Paz-Ares J, Scheible WR,Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1: 15025

Pubmed: Author and TitleCrossRef: Author and Title www.plantphysiol.orgon September 9, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Salvo-Chirnside&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Protocol: high throughput silica-based purification of RNA from Arabidopsis seedlings in a 96-well format.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Protocol: high throughput silica-based purification of RNA from Arabidopsis seedlings in a 96-well format.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Salvo-Chirnside&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schmidt S%2C Dethloff F%2C Beine%2DGolovchuk O%2C Kopka J %282013%29 The REIL1 and REIL2 proteins of Arabidopsis thaliana are required for leaf growth in the cold%2E Plant Physiol 163%3A 1623%2D1639&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmidt S, Dethloff F, Beine-Golovchuk O, Kopka J (2013) The REIL1 and REIL2 proteins of Arabidopsis thaliana are required for leaf growth in the cold. Plant Physiol 163: 1623-1639

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schmidt&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The REIL1 and REIL2 proteins of Arabidopsis thaliana are required for leaf growth in the cold&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The REIL1 and REIL2 proteins of Arabidopsis thaliana are required for leaf growth in the cold&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmidt&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schmidt S%2C Dethloff F%2C Beine%2DGolovchuk O%2C Kopka J %282014%29 REIL proteins of Arabidopsis thaliana interact in yeast%2D2%2Dhybrid assays with homologs of the yeast Rlp24%2C Rpl24A%2C Rlp24B%2C Arx1 and Jjj1 proteins%2E Plant Signal Behav 9%3A e28224&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmidt S, Dethloff F, Beine-Golovchuk O, Kopka J (2014) REIL proteins of Arabidopsis thaliana interact in yeast-2-hybrid assays with homologs of the yeast Rlp24, Rpl24A, Rlp24B, Arx1 and Jjj1 proteins. Plant Signal Behav 9: e28224

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schmidt&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=REIL proteins of Arabidopsis thaliana interact in yeast-2-hybrid assays with homologs of the yeast Rlp24, Rpl24A, Rlp24B, Arx1 and Jjj1 proteins.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=REIL proteins of Arabidopsis thaliana interact in yeast-2-hybrid assays with homologs of the yeast Rlp24, Rpl24A, Rlp24B, Arx1 and Jjj1 proteins.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmidt&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Scholl RL%2C May ST%2C Ware DH %282000%29 Seed and molecular resources for Arabidopsis%2E Plant Physiol 124%3A 1477%2D1480&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124: 1477-1480

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Scholl&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Seed and molecular resources for Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Seed and molecular resources for Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Scholl&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sch�nrock N%2C Bouveret R%2C Leroy O%2C Borghi L%2C K�hler C%2C Gruissem W%2C Hennig L %282006%29 Polycomb%2Dgroup proteins repress the floral activator AGL19 in the FLC%2Dindependent vernalization pathway%2E Genes Development 20%3A 1667%2D1678&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sch�nrock N, Bouveret R, Leroy O, Borghi L, K�hler C, Gruissem W, Hennig L (2006) Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Development 20: 1667-1678

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schönrock&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schönrock&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schulz E%2C Tohge T%2C Zuther E%2C Fernie AR%2C Hincha DK %282015%29 Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions%2E Plant Cell Environ 38%3A 1658%2D1672&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2015) Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions. Plant Cell Environ 38: 1658-1672

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schulz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schulz&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Schulz E%2C Tohge T%2C Zuther E%2C Fernie AR%2C Hincha DK %282016%29 Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana accessions%2E Sci Rep 6%3A 34027&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2016) Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana accessions. Sci Rep 6: 34027

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Schulz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana accessions.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana accessions.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schulz&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shinozaki K%2C Yamaguchi%2DShinozaki K%2C Seki M %282003%29 Regulatory network of gene expression in the drought and cold stress responses%2E Curr Opin Plant Biol 6%3A 410%2D417&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6: 410-417

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Shinozaki&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Regulatory network of gene expression in the drought and cold stress responses&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Regulatory network of gene expression in the drought and cold stress responses&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shinozaki&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Song J%2C Angel A%2C Howard M%2C Dean C %282012%29 Vernalization �?? a cold%2Dinduced epigenetic switch%2E J Cell Sci 125%3A 1%2D9&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Song J, Angel A, Howard M, Dean C (2012) Vernalization ? a cold-induced epigenetic switch. J Cell Sci 125: 1-9

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Song&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Vernalization â�?�? a cold-induced epigenetic switch&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Vernalization â�?�? a cold-induced epigenetic switch&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Song&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sormani R%2C Masclaux%2DDaubresse C%2C Daniele%2DVedele F%2C Chardon F %282011%29 Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana%2E PLoS ONE 6%3A e28070&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sormani R, Masclaux-Daubresse C, Daniele-Vedele F, Chardon F (2011) Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana. PLoS ONE 6: e28070

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sormani&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Transcriptional regulation of ribosome components are determined by stress according to cellular compartments in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sormani&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Strassburg K%2C Walther D%2C Takahashi H%2C Kanaya S%2C Kopka J %282010%29 Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress%2E OMICS J Integr Biol 14%3A 249%2D259&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Strassburg K, Walther D, Takahashi H, Kanaya S, Kopka J (2010) Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress. OMICS J Integr Biol 14: 249-259

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Strassburg&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Strassburg&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sun Q%2C Csorba T%2C Skourti%2DStathaki K%2C Proudfoot NJ%2C Dean C %282013%29 R%2DLoop stabilization represses antisense transcription at the Arabidopsis FLC locus%2E Science 340%3A 619%2D621&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013) R-Loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340: 619-621

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sun&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=R-Loop stabilization represses antisense transcription at the Arabidopsis FLC locus&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=R-Loop stabilization represses antisense transcription at the Arabidopsis FLC locus&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sun&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Thalhammer A%2C Hincha DK%2C Zuther E %282014%29 Measuring Freezing Tolerance%3A Electrolyte Leakage and Chlorophyll Fluorescence Assays%2E In%3A Hincha DK%2C Zuther E %28eds%29 Plant cold acclimation%3A Methods and Protocols%2E Methods Mol Biol 1166%3A 15%2D24&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Thalhammer A, Hincha DK, Zuther E (2014) Measuring Freezing Tolerance: Electrolyte Leakage and Chlorophyll Fluorescence Assays. In: Hincha DK, Zuther E (eds) Plant cold acclimation: Methods and Protocols. Methods Mol Biol 1166: 15-24

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thalhammer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Measuring Freezing Tolerance: Electrolyte Leakage and Chlorophyll Fluorescence Assays&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Measuring Freezing Tolerance: Electrolyte Leakage and Chlorophyll Fluorescence Assays&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thalhammer&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Thieme CJ%2C Rojas%2DTriana M%2C Stecyk E%2C Schudoma C%2C Zhang W%2C Yang L%2C Mi�ambres M%2C Walther D%2C Schulze WX%2C Paz%2DAres J%2C Scheible WR%2C Kragler F %282015%29 Endogenous Arabidopsis messenger RNAs transported to distant tissues%2E Nature Plants 1%3A 15025&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W, Yang L, Mi�ambres M, Walther D, Schulze WX, Paz-Ares J, Scheible WR, Kragler F (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1: 15025


Google Scholar: Author Only Title Only Author and Title

Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: A user-driven tool todisplay genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939


Thomashow MF (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant MolBiol 50: 571-599


Tiller N, Weingartner M, Thiele W, Maximova E, Schöttler MA, Bock R (2012) The plastid-specific ribosomal proteins of Arabidopsisthaliana can be divided into non-essential proteins and genuine ribosomal proteins. Plant J 69: 302-316


Usadel B, Nagel A, Steinhauser D, Gibon Y, Blaesing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, Fernie AR, Stitt M(2006) PageMan an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMCBioinformatics 7: 535


Van Lijsebettens M, Van der Haeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copyat the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13: 3378-3388


Walter M, Piepenburg K, Schöttler MA, Petersen K, Kahlau S, Tiller N, Drechsel O, Weingartner M, Kudla J, Bock R (2010) Knockout ofthe plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. Plant J 64: 851-863


Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate- and iron-deficientArabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 14: 783


Weis BL, Kovacevic J, Missbach S, Schleiff E (2015) Plant-specific features of ribosome biogenesis. Trends Plant Sci 20: 729-740Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends in Genetics 26: 519-527Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wu S, Tutuncuoglu B, Yan K, Brown H, Zhang Y, Tan D, Gamalinda M, Yuan Y, Li Z, Jakovljevic J, Ma C, Lei J, Dong MQ, Woolford JrJL, Gao N (2016) Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature 534: 133-137


Yamaguchi-Shinozaki K, Shinozaki K (2009) DREB regulons in abiotic-stress-responsive gene expression in plants. In: Yamada T,Spangenberg G (eds) Molecular Breeding of Forage and Turf, Springer Science & Business Media, New York, USA, pp. 15-27


Xu MY, Zhang L, Li WW, Hu XL, Wang MB, Fan YL, Zhang CY, Wang L (2014) Stress-induced early flowering is mediated by miR169 inArabidopsis thaliana. J Exp Bot 65: 89–101



http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thieme&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Endogenous Arabidopsis messenger RNAs transported to distant tissues.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Endogenous Arabidopsis messenger RNAs transported to distant tissues.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thieme&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Thimm O%2C Bl�sing O%2C Gibon Y%2C Nagel A%2C Meyer S%2C Kr�ger P%2C Selbig J%2C M�ller LA%2C Rhee SY%2C Stitt M %282004%29 MAPMAN%3A A user%2Ddriven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes%2E Plant J 37%3A 914%2D939&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Thimm O, Bl�sing O, Gibon Y, Nagel A, Meyer S, Kr�ger P, Selbig J, M�ller LA, Rhee SY, Stitt M (2004) MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thimm&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thimm&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Thomashow MF %281999%29 Plant cold acclimation%3A Freezing tolerance genes and regulatory mechanisms%2E Annu Rev Plant Physiol Plant Mol Biol 50%3A 571%2D599&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Thomashow MF (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50: 571-599

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thomashow&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thomashow&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tiller N%2C Weingartner M%2C Thiele W%2C Maximova E%2C Sch�ttler MA%2C Bock R %282012%29 The plastid%2Dspecific ribosomal proteins of Arabidopsis thaliana can be divided into non%2Dessential proteins and genuine ribosomal proteins%2E Plant J 69%3A 302%2D316&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tiller N, Weingartner M, Thiele W, Maximova E, Sch�ttler MA, Bock R (2012) The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. Plant J 69: 302-316

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tiller&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tiller&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Usadel B%2C Nagel A%2C Steinhauser D%2C Gibon Y%2C Blaesing OE%2C Redestig H%2C Sreenivasulu N%2C Krall L%2C Hannah MA%2C Poree F%2C Fernie AR%2C Stitt M %282006%29 PageMan an interactive ontology tool to generate%2C display%2C and annotate overview graphs for profiling experiments%2E BMC Bioinformatics 7%3A 535&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Usadel B, Nagel A, Steinhauser D, Gibon Y, Blaesing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, Fernie AR, Stitt M (2006) PageMan an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7: 535

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Usadel&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=PageMan an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=PageMan an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Usadel&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Van Lijsebettens M%2C Van der Haeghen R%2C De Block M%2C Bauw G%2C Villarroel R%2C Van Montagu M %281994%29 An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems%2E EMBO J 13%3A 3378%2D3388&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Van Lijsebettens M, Van der Haeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13: 3378-3388

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Van&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Van&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Walter M%2C Piepenburg K%2C Sch�ttler MA%2C Petersen K%2C Kahlau S%2C Tiller N%2C Drechsel O%2C Weingartner M%2C Kudla J%2C Bock R %282010%29 Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency%2E Plant J 64%3A 851%2D863&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Walter M, Piepenburg K, Sch�ttler MA, Petersen K, Kahlau S, Tiller N, Drechsel O, Weingartner M, Kudla J, Bock R (2010) Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency. Plant J 64: 851-863

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Walter&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Knockout of the plastid RNase E leads to defective RNA processing and chloroplast ribosome deficiency&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Walter&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang J%2C Lan P%2C Gao H%2C Zheng L%2C Li W%2C Schmidt W %282013%29 Expression changes of ribosomal proteins in phosphate%2D and iron%2Ddeficient Arabidopsis roots predict stress%2Dspecific alterations in ribosome composition%2E BMC Genomics 14%3A 783&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 14: 783

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Weis BL%2C Kovacevic J%2C Missbach S%2C Schleiff E %282015%29 Plant%2Dspecific features of ribosome biogenesis%2E Trends Plant Sci 20%3A 729%2D740&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Weis BL, Kovacevic J, Missbach S, Schleiff E (2015) Plant-specific features of ribosome biogenesis. Trends Plant Sci 20: 729-740

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Weis&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant-specific features of ribosome biogenesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant-specific features of ribosome biogenesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Weis&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wellmer F%2C Riechmann JL %282010%29 Gene networks controlling the initiation of flower development%2E Trends in Genetics 26%3A 519%2D527&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends in Genetics 26: 519-527

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wellmer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Gene networks controlling the initiation of flower development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Gene networks controlling the initiation of flower development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wellmer&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wu S%2C Tutuncuoglu B%2C Yan K%2C Brown H%2C Zhang Y%2C Tan D%2C Gamalinda M%2C Yuan Y%2C Li Z%2C Jakovljevic J%2C Ma C%2C Lei J%2C Dong MQ%2C Woolford Jr JL%2C Gao N %282016%29 Diverse roles of assembly factors revealed by structures of late nuclear pre%2D60S ribosomes%2E Nature 534%3A 133%2D137&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wu S, Tutuncuoglu B, Yan K, Brown H, Zhang Y, Tan D, Gamalinda M, Yuan Y, Li Z, Jakovljevic J, Ma C, Lei J, Dong MQ, Woolford Jr JL, Gao N (2016) Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature 534: 133-137

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yamaguchi%2DShinozaki K%2C Shinozaki K %282009%29 DREB regulons in abiotic%2Dstress%2Dresponsive gene expression in plants%2E In%3A Yamada T%2C Spangenberg G %28eds%29 Molecular Breeding of Forage and Turf%2C Springer Science %26 Business Media%2C New York%2C USA%2C pp%2E 15%2D27&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yamaguchi-Shinozaki K, Shinozaki K (2009) DREB regulons in abiotic-stress-responsive gene expression in plants. In: Yamada T, Spangenberg G (eds) Molecular Breeding of Forage and Turf, Springer Science & Business Media, New York, USA, pp. 15-27

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yamaguchi-Shinozaki&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=DREB regulons in abiotic-stress-responsive gene expression in plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=DREB regulons in abiotic-stress-responsive gene expression in plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamaguchi-Shinozaki&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Xu MY%2C Zhang L%2C Li WW%2C Hu XL%2C Wang MB%2C Fan YL%2C Zhang CY%2C Wang L %282014%29 Stress%2Dinduced early flowering is mediated by miR169 in Arabidopsis thaliana%2E J Exp Bot 65%3A 89�??101&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xu MY, Zhang L, Li WW, Hu XL, Wang MB, Fan YL, Zhang CY, Wang L (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65: 89?101

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Xu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


Documents

2 3 correspondence should be sent to - Plant …...2018/01/30 · 126 Associated with ribosomal export complex1 (Arx1) and ARX1 little brother1 (Alb1) (Lo et al., 127 2010; Meyer