Thioredoxin-Mediated ROS Homeostasis Explains …...The work was supported by the National Natural Science Foundation of China (31270231, 10 91217308). 11 12 2 These authors contributed

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Thioredoxin-mediated ROS Homeostasis Explains Natural Variation in 1

Plant Regeneration 2

Hui Zhang2, Ting Ting Zhang2, Hui Liu2, De Ying Shi, Meng Wang, Xiao Min Bie, Xing Guo Li*, 3

and Xian Sheng Zhang* 4

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State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, 6

Tai’an, 271018, China 7

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1The work was supported by the National Natural Science Foundation of China (31270231, 9

91217308). 10

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2 These authors contributed equally to this work. 12

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* Address correspondence to [email protected] and [email protected]. 14

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X.S.Z., X.G.L. and H.Z. conceived and designed the experiments; H.Z., T.T.Z., H.L., D.Y.S., M.W. 16

and X.M.B. performed the experiments; X.S.Z. and X.G.L. analyzed data and wrote the article. 17

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Short title: Regulation of Thioredoxin in Plant Regeneration 19

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One sentence summary: Thioredoxin-dependent redox modification regulates plant regeneration 21

via modulation of ROS homeostasis. 22

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Plant Physiology Preview. Published on July 19, 2017, as DOI:10.1104/pp.17.00633

Copyright 2017 by the American Society of Plant Biologists

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Plant regeneration is fundamental to basic research and agricultural applications. The regeneration 29

capacity of plants varies largely in different genotypes, but the reason for this variation remains 30

elusive. Here, we identified a novel thioredoxin DCC1 in determining the capacity of shoot 31

regeneration among Arabidopsis natural variation. Loss-of-function of DCC1 resulted in inhibited 32

shoot regeneration. DCC1 was mainly expressed in the inner tissues of the callus and encoded a 33

functional thioredoxin that was localized in the mitochondria. DCC1 protein directly interacted with 34

CARBONIC ANHYDRASE 2 (CA2), which is an essential subunit of respiratory chain NADH 35

dehydrogenase complex (Complex I). DCC1 regulated Complex I activity via redox modification of 36

CA2 protein. Mutation of DCC1 or CA2 led to reduced Complex I activity and triggered 37

mitochondrial reactive oxygen species (ROS) production. The increased ROS level regulated shoot 38

regeneration by repressing expression of the genes involved in multiple pathways. Furthermore, 39

linkage disequilibrium analysis indicated that DCC1 was a major determinant of the natural 40

variation in shoot regeneration among Arabidopsis ecotypes. Thus, our study firstly uncovers a 41

novel regulatory mechanism that thioredoxin-dependent redox modification regulates de novo shoot 42

initiation via modulation of ROS homeostasis, and provides new insights into improving the 43

capacity of plant regeneration. 44

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Plant cells have the capacity to regenerate new shoots from highly differentiated tissues or organs 59

under suitable conditions, a process known as shoot regeneration (Birnbaum and Alvarado, 2008; 60

Duclercq et al., 2011). Shoot regeneration normally includes two steps (Ikeuchi et al., 2016). The 61

first step is callus formation, which is regulated by a number of transcription factors, such as 62

WUSCHEL RELATED HOMEOBOX5 (WOX5), WOX11 and WOX12 (Sugimoto et al., 2010; Liu 63

et al., 2014), PLETHORA (PLT) (Kareem et al., 2015), LATERAL ORGAN BOUNDARIES 64

DOMAIN (LBD) (Fan et al., 2010), and WOUND INDUCED DEDIFFERENTIATION 1 (WIND1) 65

(Iwase et al., 2011). The second step is shoot induction from the callus, which consists of several 66

critical events, such as the appropriate distribution of phytohormones, shoot meristem initiation and 67

organ formation (Cheng et al., 2013; Ikeuchi et al., 2016). One of the most important events in the 68

second step is the induction of the organizing center regulator WUSCHEL (WUS), which is 69

controlled by the interaction between auxin and cytokinin (Gordon et al., 2007; Cheng et al., 2013). 70

The correct distribution of auxin and cytokinin is essential for WUS induction during de novo shoot 71

regeneration (Cheng et al., 2013). Importantly, two recent studies have shown that cytokinin 72

directly activates WUS expression by the B-type ARABIDOPSIS RESPONSE REGULATORS 73

(ARRs) (Meng et al., 2017; Zhang et al., 2017). 74

Shoot regeneration is very valuable in genetic engineering and agricultural applications, but most 75

plant species cannot regenerate shoots from highly differentiated tissues or organs (Birnbaum and 76

Alvarado, 2008). Even in the same species, the shoot regeneration capacity varies among different 77

genotypes (Motte et al., 2014). However, the mechanisms underlying this natural variation in shoot 78

regeneration capacity remains unclear. Several studies have identified a few quantitative trait loci 79

related to natural variations in shoot regeneration (Schiantarelli et al., 2001; Lall et al., 2004; 80

Velázquez et al., 2004). A recent study has shown that RECEPTOR-LIKE PROTEIN KINASE1 81

(RPK1) gene is involved in natural variation in shoot regeneration capacity (Motte et al., 2014). 82

Further identification of the critical genes that control shoot regeneration and how they vary among 83

different genotypes are required for research in both the mechanisms and applications of shoot 84

regeneration. 85

Reactive oxygen species (ROS) are crucial signaling molecules that can alter their target proteins 86

activity by oxidative posttranslational modifications (Waszczak et al., 2015). Many proteins that act 87

in hormonal signal perception and response, MAPK signal transduction, and influx channel pathway, 88



4

are redox sensitive to ROS (Waszczak et al., 2015; Kimura et al., 2017). Altered levels of ROS lead 89

to change the activity of these target proteins and affect various developmental processes (Schippers 90

et al., 2016). During root development, ROS homeostasis is critical for the transition from cell 91

proliferation to cell differentiation (Tsukagoshi et al., 2010). High levels of ROS result in reduced 92

root meristem activity (Tsukagoshi et al., 2010), and small leaf size (Lu et al., 2014). ROS is also 93

involved in regulating polar growth of pollen and root hairs (Mangano et al., 2016), and senescence 94

of leaf and flower (Rogers and Munné-Bosch, 2016). In addition, ROS is generated in various 95

subcellular compartments. Chloroplasts (Dietz et al., 2016), mitochondria (Huang et al., 2016), and 96

peroxisomes (Sandalio and Romero-Puertas, 2015), are the major producers of ROS in plant cells. 97

ROS homeostasis is governed by diverse antioxidant factors (Considine and Foyer, 2014; Lu and 98

Holmgren, 2014). Thioredoxins (Trxs) are key actors to modulate ROS scavenging, and functional 99

loss of Trx results in altered ROS levels (Dos Santos and Rey, 2006; Schippers et al., 2016). Trxs 100

are widely distributed proteins with a main function to reduce specific S-S group through a 101

conserved motif CxxC (Gelhaye et al., 2005; Meyer et al., 2005). Trxs alter the activity of 102

interacting target proteins via thiol-based redox modifications (Rouhier et al., 2015). A number of 103

potential Trx targets have been identified using proteomic approaches (Montrichard et al., 2009). 104

Trxs can affect diverse signaling pathways by modulating the activity of their target proteins, such 105

as enzymes of peroxiredoxins (Prxs) and glutathione peroxidase (Gpxs) for ROS scavenging (Dos 106

Santos and Rey, 2006), transcription factors for gene expression (Murmu et al., 2010; Viola et al., 107

2013), and hormonal receptors for signal transduction (Tada et al., 2008). Mitochondrial respiratory 108

chain NADH dehydrogenase complex (Complex I) consists of several essential subunits and is one 109

of the major sites of electron entry into the electron transport chain (ETC) in the process of ATP 110

production (Braun et al., 2014). Altered redox state of the subunits results in reduced Complex I 111

activity (Galkin et al., 2008). Proteomic analyses have revealed that many subunits of Complex I 112

are potential targets of Trxs, suggesting a crucial role for Trxs in regulating mitochondrial Complex 113

I function (Balmer et al., 2004; Yoshida et al., 2013; Braun et al., 2014; Dröse et al., 2014). 114

However, the evidence that Trxs directly regulate these subunits remains missing. Redox of Trxs 115

regulates diverse developmental processes, such as embryo formation, leaf development, and 116

maintenance of meristem activity (Benitez-Alfonso et al., 2009; Bashandy et al., 2010; Meng et al., 117

2010). Here, we showed that thioredoxin-dependent redox modification regulated de novo shoot 118



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initiation via modulation of ROS homeostasis. The study provides novel information for 119

understanding the mechanisms of natural variation in plant regeneration. 120

RESULTS 121

Loss-of-Function of DCC1 Results in Inhibition of Shoot Regeneration 122

To determine the function of thioredoxins in shoot regeneration, seven T-DNA insertion mutants 123

of Trx (Trx O1, Trx O2, Trx H1, Trx H2, Trx H5, AT5G50100, AT1G52590) from the Arabidopsis 124

Biological Resource Center (ABRC) were screened, but only SALK_051222C (AT5G50100) mutant 125

showed severe defects in shoot regeneration (Supplemental Table S1). This mutant contained a 126

T-DNA insert in the fourth intron of AT5G50100 (Supplemental Fig. S1A). Reverse transcription 127

PCR (RT-PCR) analyses showed that the transcript level of this gene was decreased in this mutant 128

(Supplemental Fig. S1B), suggesting that the T-DNA insertion leads to reduced levels of functional 129

transcripts. AT5G50100 encodes a protein in the thiol-disulfide oxidoreductase family, whose 130

members contain a conserved DxxCxxC motif in their N-terminus (Ginalski et al., 2004). In 131

Arabidopsis, there exist three members with DxxCxxC motif, but their functions have not been 132

determined. Thus, At5g50100 was designated as DCC1. 133

Loss-of-function of DCC1 resulted in a decreased capacity for shoot regeneration, including the 134

low shoot regeneration frequency and the small number of shoots per callus (Fig. 1, A–C). 135

Wild-type callus generated shoots on shoot-induction medium (SIM) at 16 days (Fig. 1, A and B), 136

but the dcc1 mutant callus took 20 days to produce shoots (Fig. 1, A and B). The shoot regeneration 137

frequency in wild-type Columbia-0 (Col-0) was 100% at 28 days on SIM, while that of dcc1 was 138

about 30% (Fig. 1, A and B). The number of shoots per callus was significantly lower in dcc1 than 139

in wild type (Fig. 1, A and C). Furthermore, the phenotypes of the frequencies of shoot regeneration 140

and the shoot number per callus caused by mutation of DCC1 were both rescued by the 141

transformation of the complementary construct ProDCC1:DCC1 into dcc1 mutant (Fig. 1, A–C). 142

Thus, these results indicate that mutation of DCC1 leads to an inhibition of shoot regeneration. 143

Furthermore, we showed that DCC1 was mainly expressed in the inner region of the callus during 144

shoot regeneration by both in situ hybridization (Fig. 1D) and beta-Glucuronidase (GUS) analyses 145

(Fig. 1E). 146

DCC1 Encodes a Functional Thioredoxin Localized in Mitochondria 147



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DCC1 contained an N-terminal DxxCxxC motif in a function-unknown DUF393 domain (in 148

Pfam database) (Fig. 2A). The DxxCxxC motif is a conserved signature sequence for DCC family 149

proteins in various species, but not in animals (Fig. 2B). Phylogenetic analysis indicated that DCC1 150

shared high homology with several proteins in species, such as Camelina sativa, Brassica rapa and 151

Raphanus sativus (Fig. 2C). The presence of two cysteine residues in DxxCxxC motif implied a 152

function for DCC1 in regulating thiol-disulfide exchange. Thus, we performed a Trx activity 153

detection assay using fluorescein isothiocyanate-labeled insulin (FiTC-insulin). FiTC-insulin is a 154

highly sensitive substrate for the measurements of Trx activity and displays higher fluorescence 155

after disulfide reduction (Montano et al., 2014). The reduction assay was performed by incubation 156

with purified DCC1 protein and a high fluorescence intensity was achieved, whereas the control 157

without DCC1 protein showed a low level of insulin reduction (Fig. 2D), confirming its activity as a 158

functional thioredoxin. 159

DCC1 contained a mitochondrial signal sequence, implying it might be localized in the 160

mitochondria (Fig. 2A). To test this hypothesis, we obtained a well-established marker line MT-GK 161

specially expressing GFP in mitochondria (Mito-GFP) (Nelson et al., 2007). Then, the construct 162

35S:DCC1-RFP was introduced into the MT-GK lines. The roots of the T1 seedlings were used for 163

imaging by a laser confocal microscopy. The DCC1-RFP signal was co-localized with the 164

Mito-GFP signal of the control mitochondrion marker (Fig. 2E), indicating that DCC1 is localized 165

in mitochondria. 166

DCC1 Directly Interacts with CA2 167

To uncover the functional pathway of DCC1 in shoot regeneration, we searched for its potential 168

target(s). We analyzed the published proteome-wide binary protein–protein interaction map 169

constructed by yeast two-hybrid assay in Arabidopsis thaliana, and found a DCC1 potential 170

interaction target CARBONIC ANHYDRASE 2 (CA2) (Arabidopsis Interactome Mapping 171

Consortium, 2011), which is a beta carbonic anhydrase (Soto et al., 2015). CA2, together with other 172

four carbonic anhydrases (CA1, CA3, CAL1 and CAL2), constitutes a functional subunit of 173

mitochondrial respiratory complex I (Soto et al., 2015). By a yeast two-hybrid assay, we found that 174

only the yeast co-transformed with DCC1-AD and CA2-BD constructs could survive on selection 175

medium (Fig. 3A). In pull-down assays using the purified proteins of DCC1 and CA2, an obvious 176

lane of DCC1-His was observed (Fig. 3B). To further confirm the interaction between DCC1 and 177



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CA2 in vivo, we co-transformed the constructs DCC1-nLUC and CA2-cLUC into Nicotiana 178

benthamiana leaves, and observed high fluorescence intensity compared with that in the controls 179

(Fig. 3C). In DCC1-GFP immunoprecipitation assays of the F1 generation of 35S:DCC1-GFP line 180

crossed with 35S:CA2-MYC line, we detected an obvious lane of the CA2-MYC protein (Fig. 3D), 181

indicating an interaction between DCC1 and CA2. 182

Mutation of CA2 Causes the Decreased Shoot Regeneration Capacity 183

To determine the function of CA2 in shoot regeneration, we obtained the T-DNA insertion mutant 184

ca2 and analyzed its shoot regeneration capacity. The mutation of CA2 led to a significantly 185

decreased shoot regeneration capacity. During shoot regeneration, the shoots started to emerge at 16 186

days on SIM in wild type, whereas the mutant callus generated shoots at 20 days on SIM (Fig. 4A). 187

The shoot regeneration frequency of wild type reached 100% at 28 days after transfer of calli onto 188

SIM, while that of ca2 was only about 40% (Fig. 4B). The number of shoots per callus showed a 189

similar inhibition (Fig. 4C). The frequencies of shoot regeneration and the shoot number per callus 190

were completely rescued by the transformation of the complementary construct ProCA2:CA2 into 191

the ca2 mutant (Fig. 4, A–C). Next, we crossed the two single mutants, and obtained the 192

homozygous double mutant dcc1ca2. The double mutant dcc1ca2 showed similar phenotypes with 193

those in dcc1 mutant in terms of inhibited shoot regeneration (Supplemental Fig. 2, A-C). 194

Furthermore, we detected the spatiotemporal expression patterns of CA2, and showed that CA2 195

expression in the callus started at 8 days on SIM, and gradually increased in the inner region of the 196

callus (Fig. 4, D and E). 197

Mutation of DCC1 or CA2 Leads to Reduced Complex I Activity and Increased ROS Level 198

DCC1 was a functional thioredoxin and directly interacted with CA2 protein, implying that CA2 199

might be reduced by DCC1. Therefore, we performed a reduction assay by using purified 200

recombinant CA2 protein as the substrate. CA2 was incubated with or without GST cleaved 201

recombinant DCC1 protein. DTT (0.3mM) was added to recycle DCC1 activity. The reduction of 202

CA2 was monitored by the mobility shift in nonreducing SDS-PAGE. CA2 contained two cysteine 203

residues (Cys-83 and Cys-137) and formed dimmer and oligomer complexes by intermolecular 204

disulfide bonds (Fig. 5, A and B). The intensity of CA2 complex lanes showed significantly 205

decreased after incubation with DCC1 protein (Fig. 5, A and B), suggesting DCC1 promotes 206

monomer formation by reduction of CA2 complex. 207



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CA2 is a key subunit of the mitochondrial respiratory complex I, and defect in CA2 leads to 208

decreased activity of complex I (Soto et al., 2015). Thus, we detected the activity of respiratory 209

complex I in dcc1, ca2, and dcc1ca2 during shoot regeneration. Functional loss of DCC1 or CA2 210

caused a significantly decreased activity of the mitochondrial respiratory complex I (Fig. 5C). The 211

complex I activity in the double mutant dcc1ca2 was not more affected than that in the single 212

mutants, indicating that both proteins are acting in the same pathway. Furthermore, the reduced 213

activity of Complex I in the dcc1ca2 double mutant was completely rescued by both additions of 214

DCC1 and CA2 proteins, but not for only addition of DCC1 or CA2 (Fig. 5D). These results 215

suggest that DCC1 affects complex I activity via redox regulation of CA2 protein. Previous study 216

has shown that the impaired activity of respiratory complex I results in increased ROS levels (Soto 217

et al., 2015). Thus, we hypothesize that the reduced mitochondrial respiratory complex I activity 218

triggers mitochondrial ROS production. To test this hypothesis, we performed DAB staining assays 219

to detect the ROS levels in callus (Xie et al., 2014). During shoot regeneration, functional loss of 220

DCC1 or CA2 resulted in increased ROS levels in calli cultured on CIM and SIM, respectively (Fig. 221

6, A and B). The ROS level in the double mutant dcc1ca2 was consistent to that in either single 222

mutant (Fig. 6, A and B). 223

ROS Levels Mediate Inhibition of Shoot Regeneration 224

Since the loss-of-function of DCC1 and CA2 resulted in increased ROS levels, we thought that 225

the inhibition of shoot regeneration in the dcc1 or ca2 mutant might be due to increased ROS levels. 226

To test this hypothesis, we treated explants of wild type with exogenous H2O2, a well-demonstrated 227

regent responsible for increasing ROS levels (Yu et al., 2016), and found that shoot regeneration 228

was significantly inhibited in the treated explants (Fig. 7, A-C). Moreover, higher levels of H2O2 led 229

to lower shoot regeneration capacities (Fig. 7, A-C). The wild type without H2O2 treatment 230

generated visible shoots at 16 days on SIM, whereas wild type treated with 0.005‰ H2O2 and 231

0.01‰ H2O2 generated shoots at 20 days on SIM (Fig. 7A). At 28 days on SIM, the wild type 232

without H2O2 treatment had a shoot regeneration frequency of 100% (Fig. 7B), whereas wild type 233

treated with 0.005‰ H2O2 and 0.01‰ H2O2 had shoot regeneration frequencies of 70% and 30%, 234

respectively (Fig. 7B). The number of shoots regenerated from wild-type calli was also decreased 235

when treated with exogenous H2O2 (Fig. 7C), indicating that ROS inhibits shoot regeneration. 236

Next, we determined whether glutathione (GSH), the main endogenous antioxidant responsible 237



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for ROS removal (Lu and Holmgren, 2014), could rescue the phenotypes of dcc1 and ca2 by 238

decreased the ROS levels. The frequencies of shoot regeneration in the dcc1, ca2, and dcc1ca2 239

mutants were increased with gradually increasing concentrations of GSH (Supplemental Fig. S3A). 240

The number of shoots per callus showed similar increases under GSH treatment (Supplemental Fig. 241

S3B). The dcc1, ca2, and dcc1ca2 mutants were completely rescued by GSH at 600 µM (Fig. 8, 242

A–C). Although the shoot regeneration promoted in the wild type by GSH, the shoot regeneration in 243

the mutants of dcc1, ca2 and dcc1ca2 by GSH was significantly increased compared with that in the 244

wild type (Fig. 8, A-C). These results indicate that the reduction of ROS levels by GSH promotes 245

shoot regeneration. To further confirm the function of ROS in shoot regeneration, we transformed 246

the construct pER8-CAT3, which overexpressed CATALASE 3 (CAT3) when induced with estradiol, 247

into the Col-0, dcc1, ca2, and dcc1ca2 mutants. CAT3 encodes a catalase, which catalyzes the 248

breakdown of H2O2 into water and oxygen, thereby reduces the H2O2 level (Zou et al., 2015). The 249

CAT3 overexpression transgenic lines were obtained in the backgrounds of Col-0, dcc1, ca2, and 250

dcc1ca2, respectively (Supplemental Fig. S4). The shoot regeneration frequencies and number of 251

shoots per callus were increased in the CAT3-overexpressing transgenic lines (Fig. 8, A-C), 252

indicating that the reduction in ROS levels by overexpression of CAT3 rescued the phenotypes of 253

the mutants. CAT3 overexpression in Col-0 led to about two more shoots per callus than Col-0, 254

whereas CAT3 overexpression in dcc1, ca2 and dcc1ca2 mutants showed about five more shoots 255

compared with their mutants, respectively. Thus, the results confirm that the ROS level is critical 256

for regulating the shoot regeneration capacity. 257

ROS Regulates Shoot Regeneration by Modulating Multiple Pathways 258

Shoot regeneration includes callus formation and shoot meristem induction. To determine 259

whether ROS was involved in regulation of callus formation by master regulators, we analyzed 260

WOXs, PLTs, LBDs and WIND1 expression during this process. Only WOX5 and WOX11 showed 261

the reduced levels in dcc1 mutant (Fig. 9A), suggesting ROS affects callus formation by modulation 262

of WOX5 and WOX11 expression. Next, we detected the WUSCHEL (WUS), SHOOT 263

MERISTEMLESS (STM) and CLAVATA3 (CLV3) which are involved in shoot meristem induction 264

(Ikeuchi et al., 2016). The transcript levels of all the three genes were decreased in dcc1 mutant 265

cultured on SIM at 12 days and 16 days (Fig. 9B), suggesting that ROS regulates shoot induction by 266

modulating expression of WOXs, WUS, CLV3 and STM. 267



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To uncover the functional pathways of ROS in detail, we performed a RNA-seq analysis using 268

the calli of wild type (Col-0) and dcc1 cultured on SIM at 16 days. Three high-quality biological 269

repeats of wild type (Col-0-A, Col-0-B, Col-0-C) and dcc1 (dcc1-A, dcc1-B, dcc1-C) were used for 270

RNA-seq analyses (Supplemental Fig. S5). Using a two-fold change in the gene transcript levels 271

between the wild-type Col-0 and the mutant dcc1 with an adjusted P value (FDR) cut-off of 0.05 as 272

the criterion for differential expression, we identified many differentially expressed genes (Fig. 273

10A). Among them, 689 genes were up-regulated and 2332 genes were down-regulated in dcc1 (Fig. 274

10A; Supplemental Tables S2 and S3). Gene Ontology (GO) analyses showed that DCC1 regulated 275

multiple processes such as auxin biosynthetic process (P = 1.38 × 10-3), shoot system development 276

(P = 6.33 × 10-15), oxidation–reduction process (P = 1.83 × 10-13), cell differentiation (P = 1.98 × 277

10-11), response to hormones (P = 2.88 × 10-9), cell wall organization (P = 2.24 × 10-8), organ 278

morphogenesis (P = 1.94 × 10-7), and hydrogen peroxide catabolic process (P = 4.35 × 10-5) (Fig. 279

10B). In addition to WUS and STM, the meristem master genes KNOTTED-LIKE FROM 280

ARABIDOPSIS THALIANA1 (KNAT1), KNAT2, KNAT4 (Scofield et al., 2007), WUSCHEL 281

RELATED HOMEOBOX (WOXs) (van der Graaff et al., 2009), and CUP-SHAPED COTYLEDON 282

(CUCs) (Ikeuchi et al., 2016), were down-regulated in dcc1 (Fig. 10, B and C). Next, we performed 283

quantitative reverse transcription PCR (qRT-PCR) to confirm the transcript levels of genes 284

identified in the RNA-seq analyses. As expected, the transcript levels of these genes were low in 285

dcc1 mutant, and in the presence of exogenous H2O2 (Fig. 10D; Supplemental Fig. S6). These 286

results suggest that DCC1-mediated ROS level regulates shoot regeneration by the genes involved 287

in shoot meristem initiation. 288

Interestingly, several auxin biosynthetic genes, including TRYPTOPHAN AMINOTRANSFERASE 289

OF ARABIDOPSIS 1 (TAA1), YUCCA2 (YUC2), YUC4, YUC5, and YUC9 (Zhao, 2010) were 290

significantly down-regulated in dcc1 (Fig. 10, C and D; Supplemental Fig. S6). The transcript levels 291

of auxin response genes, such as GRETCHEN HAGEN 3.6 (GH3.6) and SMALL AUXIN 292

UPREGULATED 51 (SAUR51) (Hagen and Guilfoyle, 2002; Staswick et al., 2005), were also 293

decreased in dcc1 (Fig. 10, C and D; Supplemental Fig. S6). Further, we used the 294

well-demonstrated auxin marker DR5rev:GFP to detect the auxin response signal distribution in 295

regenerating shoots (Cheng et al., 2013). The GFP signal was weakened by H2O2 treatment during 296

shoot regeneration (Fig. 10E). Auxin is a critical determinant in shoot regeneration, and the 297



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impaired auxin biosynthesis and signaling repress shoot regeneration (Gordon et al., 2007; Cheng et 298

al., 2013). Moreover, the functional loss of DCC1 led to increased ROS levels (Fig. 6, A and B), and 299

ROS repressed auxin signaling (Fig. 10E). Thus, we propose that DCC1-mediated ROS level 300

regulates shoot regeneration, at least in part, through a modulation of the auxin biosynthesis and 301

signaling pathway. 302

DCC1 Is a Major Determinant of Natural Variation in Shoot Regeneration 303

To determine whether DCC1 was a factor in the natural variation in shoot regeneration, 304

forty-eight ecotypes of Arabidopsis were used in shoot regeneration analyses using the roots as 305

explants. The shoot regeneration capacity varied widely among the different ecotypes of 306

Arabidopsis. The shoot regeneration frequencies ranged from 5% to 100% (Supplemental Fig. S7A). 307

The ecotypes Gu-0, Nc-1, Wa-1, and Kelsterbach-4 showed very low shoot regeneration frequencies 308

on SIM at 28 days, while the ecotypes Col-0, Ws-0, Pu2-7, Lan-0, and Bu-0 showed high shoot 309

regeneration frequencies (Supplemental Fig. S7A). These diverse frequencies indicated the wide 310

natural variation in regeneration capacity among Arabidopsis genotypes. There was also a wide 311

range among genotypes in the number of shoots per callus (Supplemental Fig. S7B). Each callus of 312

Col-0, Ws-0, Pu2-7, Bu-0, Tsu-1 and Ct-1 generated more than five shoots, while calli of other 313

ecotypes generated four or fewer. The results confirm that there are diverse shoot regeneration 314

capacities among different ecotypes of Arabidopsis. 315

We further performed linkage disequilibrium analyses using the nucleotide sequences of DCC1 in 316

48 different ecotypes, and found that six SNPs (SNP 108, 147, 174, 175, 378, and 481) were highly 317

associated with the shoot regeneration frequency (Fig. 11A). Two haplotypes (Hap1 and Hap2) of 318

DCC1 were identified among 48 natural variants of Arabidopsis. Hap1 included 30 ecotypes such 319

as Col-0, Ws-0, Pu2-7, Lan-0, and Bu-0, and Hap2 included 18 ecotypes such as Gu-0, Nc-1, 320

Keleterbach-4, Hn-0, Su-0 (Fig. 11, A-C). The shoot regeneration frequencies and the number of 321

shoots per callus were much higher in the Hap1 than in the Hap2 ecotypes (Fig. 11, D and E), 322

suggesting that this natural variation in DCC1 is related to the regulation of shoot regeneration. 323

Among the six SNPs, only two (SNP 175 and 481) resulted in the sense mutation (I59V and I161V) 324

for the corresponding amino acids (Fig. 11, B and C). To identify the critical SNPs in DCC1 among 325

the natural variants, we detected the Trx activity by reduction of FiTC-insulin. Mutations at both 326

175 and 481 sites did not affect Trx activity of DCC1 (Fig. 11, F and G). Next, we performed yeast 327



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two-hybrid assays using the DCC1 with mutations at 175 and 481 sites. We found that DCC1 did 328

not interact with CA2 when there were mutations at both sites 175 and 481 (Fig. 11H). We also 329

transformed a pDCC1:DCC1-m175-m481 construct with DCC1 mutated at 175 and 481 sites to 330

rescue dcc1 mutant. The shoot regeneration frequencies in the pDCC1:DCC1-m175-m481-dcc1 331

transgenic lines were not significantly different from those in dcc1 (Fig. 11I), implying that SNP 332

175 and SNP 481 of DCC1 are critical for shoot regeneration. 333

Because DCC1 regulated shoot regeneration through ROS level, we assumed that 334

DCC1-mediated ROS homeostasis might be involved in the natural variation in shoot regeneration 335

among Arabidopsis ecotypes. To test this hypothesis, we detected the ROS levels in the Hap1 and 336

Hap2 ecotypes by DAB staining (Fig. 12, A and B). The shoot regeneration frequencies and the 337

number of shoots per callus were higher in the Hap1 ecotypes (Col-0, Kro-0, En-1, Ct-1, and Lp2-6) 338

than in the Hap2 ecotypes (Bsch-0, Aa-0, Hn-0, Kelsterbach-4, and Gu-0) (Fig. 12, C and D). 339

Interestingly, the ROS levels were significantly lower in the Hap1 ecotypes than in the Hap2 340

ecotypes (Fig. 12E). These results suggest that DCC1-mediated ROS homeostasis is critical to the 341

natural variation in shoot regeneration among Arabidopsis ecotypes. 342

DISCUSSION 343

Trxs belong to small proteins with a conserved CxxC motif throughout all organisms (Gelhaye 344

et al., 2005; Meyer et al., 2005). Classic Trxs, such as Trx m, Trx o, Trx h and Trx f, contain a motif 345

of WCGPC or WCPPC, and atypical Trxs, such as APS REDUCTASE 1 (APR1), and HIGH 346

CHLOROPHYLL FLUORESCENCE 164 (HCF164), have a motif of WCPFC, HCGPC or 347

WCEVC (Gelhaye et al., 2005; Meyer et al., 2005). Trxs catalyze the reduction of disulfide bond 348

through these motifs and are critical to change redox state of their target proteins (Rouhier et al., 349

2015). Redox state of ND3 (an important subunit of Complex I) determines activity of Complex I 350

(Galkin et al., 2008). Many subunits of mitochondrial respiratory Complex I (such as NAD7, NAD9, 351

NDS8A, and NDUV2) are identified as potential targets of Trxs, but the direct evidence of redox 352

regulation of these subunits by Trxs is missing (Balmer et al., 2004; Yoshida et al., 2013). In this 353

study, we characterized a novel atypical Trx DCC1, which belongs to DCC family proteins. These 354

proteins contain a conserved DxxCxxC motif (such as DGDCPLC, DGECPLC and DGVCHLC) 355

that differs from motifs of classic and atypical Trxs (Fig. 2B). DCC1 had the Trx activity 356



13

determined by reduction of insulin (Fig. 2D). CA2 is an essential subunit of Complex I (Soto et al., 357

2015), and was identified as a direct target of DCC1 (Fig. 5, A and B). DCC1 regulated Complex I 358

activity by reduction of CA2 complex (Fig. 5, A-D). Inhibition of Complex I activity caused by 359

mutation of DCC1 or CA2 triggered the increased ROS production (Fig. 6, A and B), suggesting 360

that DCC1 regulates Complex I activity and ROS homeostasis by redox regulation of CA2. 361

Many studies show that ROS can act as signaling factors regulating diverse processes (Rouhier et 362

al., 2015; Schmidt and Schippers, 2015; Schippers et al., 2016). NADPH-DEPENDENT 363

THIOREDOXIN REDUCTASE A (NTRA), NADPH-DEPENDENT THIOREDOXIN REDUCTASE B 364

(NTRB), and glutathione biosynthesis gene CADMIUM SENSITIVE 2 (CAD2) function to maintain 365

ROS homeostasis, and the triple mutant ntra ntrb cad2 generated an abnormal shoot meristem 366

(Bashandy et al., 2010). Higher levels of ROS caused by overexpression of UP BEAT1 (UPB1) led 367

to a short root meristem (Tsukagoshi et al., 2010). Elevated levels of ROS by the mutation of 368

KUODA1 (KUA1) led to the decreased leaf cell size (Lu et al., 2014). Here, we showed that 369

increasing level of ROS resulted in the inhibition of shoot regeneration (Fig. 6, A and B; Fig. 7, 370

A–C), whereas decreasing level of ROS level increased the capacity of shoot regeneration in the 371

mutants of dcc1, ca2, and dcc1ca2 (Fig. 8, A–C). Thus, ROS homeostasis is critical for regulation 372

of shoot regeneration. 373

Different mechanisms have been proposed to mediate perception of ROS (Wrzaczek et al., 2013). 374

An important mechanism is the one-component redox signaling system, which is based on 375

redox-sensitive transcription factors (Schmidt and Schippers, 2015). Recent studies have identified 376

a number of crucial redox-sensitive transcription factors, such as (PHAVOLUTA) PHV for 377

meristem development and organ polarity, BASIC REGION/LEUCINE ZIPPER 378

TRANSCRIPTION FACTOR 16 (bZIP16) for light signaling, and TEOSINTE 379

BRANCHED1-CYCLOIDEAPCF 15 (TCP15) for auxin signaling (Schmidt and Schippers, 2015). 380

Our results indicated that the increased ROS levels resulted in repressed expression of master genes 381

for callus formation (WOX5, WOX11), and shoot meristem initiation (WUS, CLV3 and STM) (Fig. 9, 382

A and B). Moreover, auxin biosynthesis genes (YUC4, TAA1) were repressed by ROS (Fig. 10, C 383

and D). Previously, it was shown that auxin was critical for shoot induction, and mutation of auxin 384

biosynthetic genes YUCs repressed shoot regeneration (Gordon et al., 2007; Cheng et al., 2013). 385

The redox-sensitive transcription factors TCPs regulate YUCs expression and auxin biosynthesis 386



14

(Viola et al., 2013; Lucero et al., 2015; Challa et al., 2016). Thus, it is likely that ROS regulates 387

shoot regeneration by redox modification of transcription factors involved in auxin biosynthesis and 388

signaling. 389

The evolutionary adaptation of plants to environmental changes leads to diverse natural variation, 390

which is critical for plant diversity (Mitchell-Olds and Schmitt, 2006). Natural variation causes a 391

wide range of biological phenotypes and provides rich resources to analyze many important 392

complex traits (Mitchell-Olds and Schmitt, 2006). A number of factors involved in natural 393

variations have been identified in diverse biological processes including regulation of flowering, 394

seed development, and drought resistance (Johanson et al., 2000; Li et al., 2011b; Wang et al., 2016). 395

FRIGIDA (FRI) is a major determinant of the natural variation in Arabidopsis flowering time 396

(Johanson et al., 2000). Natural variations in GS5 can explain variations in rice grain size and yield 397

(Li et al., 2011b), and those in ZmVPP1 contribute to the drought tolerance trait in Zea mays (Wang 398

et al., 2016). Here, we identified a major regulator DCC1 that explains the variation in shoot 399

regeneration capacity among natural variants of Arabidopsis (Fig. 11, A–E). The polymorphisms of 400

DCC1 were used to classify the different ecotypes of Arabidopsis into two groups: Hap1 and Hap2 401

(Fig. 11B). Interestingly, mutations at both two critical SNPs (SNP 175, SNP 481) did not affect the 402

Trx activity of DCC1 (Fig. 11G), but blocked the interaction between DCC1 and CA2 (Fig. 11H), 403

indicating that the two SNPs are critical for the function of DCC1, which is a major player in 404

determining shoot regeneration capacity among natural variations. 405

MATERIALS AND METHODS 406

Plant Materials 407

The mutants dcc1 (SALK_051222C), ca2 (SALK_010194C), MT-GK line (CS16263), and 408

different ecotypes of Arabidopsis were obtained from the Arabidopsis Biological Resource Center 409

(ABRC). DR5rev:GFP lines were generously provided by Dr. Jian Xu (Department of Biological 410

Science, National University of Singapore) (Xu et al., 2006). 411

Shoot Regeneration 412

Shoot regeneration experiment was performed as described previously (Li et al., 2011a). Seeds 413

were placed on germination medium after sterilization in 70% v/v ethanol for 5 min and 2.6% v/v 414

sodium hypochlorite for 10 min. All the seeds were stratified at 4°C for 3 days, and then grown for 415

12 days in a growth chamber at 22°C under a 16-h light/8-h dark photoperiod. Root segments (5–10 416



15

mm) were cut and placed on callus induction medium CIM (Gamborg’s B5 medium supplemented 417

with 0.5 g/L MES, 2% w/v glucose, 0.2 µM kinetin, 2.2 µM 2,4-dichlorophenoxyacetic acid, and 418

0.8% w/v agar). After the explants were incubated in continuous light for 6 days, the calli were 419

transferred onto SIM (Gamborg’s B5 medium supplemented with 0.5 g/L MES, 2% w/v glucose, 420

0.9 µM 3-indoleacetic acid, and 0.5 µM 2-isopentenyladenine, 0.8% w/v agar), and incubated in 421

continuous light. The calli were transferred onto fresh medium every 6 days. Images of calli were 422

acquired using an Olympus DP72 microscope. The shoots on each callus were defined as being at 423

least 2 mm long. Shoot regeneration frequency (%) was calculated as follows: number of calli with 424

at least one shoot / total number of calli cultured on SIM × 100. Three sets of biological replicates 425

were used in the calculations and more than 100 calli were examined in each replicate. 426

Plasmid Construction 427

The oligonucleotide primers for all constructs are given in Supplemental Table S4. For 428

phenotypic complementation and GUS signal analyses, DCC1 or CA2 genomic fragments including 429

the promoter and gene were introduced into pMDC99 to construct the ProDCC1:DCC1 and 430

ProCA2:CA2, respectively, and into the pMDC163 to obtain ProDCC1:DCC1-GUS and 431

ProCA2:CA2-GUS, respectively. For subcellular localization, DCC1 cDNA was cloned into 432

pH7RWG2 to generate 35S:DCC1-RFP by Gateway Technology (Karimi et al., 2002). For the yeast 433

two-hybrid constructs, cDNAs of DCC1 and CA2 without the signal peptide sequence were cloned 434

into the pGADT7 and pGBKT7 to generate DCC1-AD and CA2-BD, respectively. For the pull-down 435

assay, cDNAs of DCC1 and CA2 without the signal peptide sequence were cloned into pET28a and 436

pGEX-4T-1 to generate DCC1-His and CA2-GST, respectively. For the firefly luciferase 437

complementation assay, gene sequences of DCC1 and CA2 were cloned into p1300-nLUC and 438

p1300-cLUC to generate 35S:DCC1-nLUC and 35S:CA2-cLUC, respectively. For the 439

co-immunoprecipitation, gene sequences of DCC1 and CA2 were introduced into pEarlyGate103 440

and pEarlyGate203 to generate 35S:DCC1-GFP and 35S:CA2-MYC, respectively. For the reduction 441

of CA2, cDNA of DCC1 without the signal peptide sequence was cloned into pGEX-4T-1 to 442

generate DCC1-GST. For CAT3-overexpression, CAT3 cDNA was amplified and cloned into the 443

pER8 to construct pER8-CAT3. 444

For the construct pDCC1:DCC1-m175-m481, DCC1 promoter sequence was amplified using 445

the primer DCC1-F7/R7 and cloned into pBI121. DCC1-m175-m481 (m175 indicates mutation at 446



16

175 site of DCC1 gene) fragments were amplified using primers (DCC1-F8/R8, DCC1-F9/R9, 447

DCC1-F10/R10) by over-lap-extension two-step PCR mutagenesis method, and introduced into the 448

pBI121 containing DCC1 promoter. For DCC1 Trx activity determination, DCC1-m175-His (with 449

primer DCC1-F11/R11), DCC1-m481-His (with primers DCC1-F12/R12, DCC1-F13/R13), and 450

DCC1-m175-m481-His (with primers DCC1-F11/R12, DCC1-F13/R13) were generated by 451

over-lap-extension two-step PCR mutagenesis and inserted into pET28a for protein purification. For 452

yeast hybrid interaction, DCC1-m175-AD (with primer DCC1-F14/R14), DCC1-m481-AD (with 453

primers DCC1-F15/R15, DCC1-F16/R16), and DCC1-m175-m481-AD (with primers 454

DCC1-F14/R15, DCC1-F16/R16) were amplified by over-lap-extension two-step PCR mutagenesis 455

and inserted to pGADT7 for yeast hybrid interaction. 456

GUS Staining Assay 457

We conducted GUS staining assays as described elsewhere (Sieburth and Meyerowitz, 1997; Su 458

et al., 2009). Briefly, calli were incubated in GUS assay buffer at 37°C for 10 h, and fixed in 70% 459

v/v ethanol at room temperature. The calli were embedded in paraffin and cut into 10-μm sections. 460

Ruthenium red (0.2 g/L) was used to stain cell walls. 461

Confocal Microscopy 462

MT-GK is a reported marker line specially expressing GFP in mitochondria (Mito-GFP) (Nelson 463

et al., 2007). To determine the subcellular localization of DCC1, the construct 35S:DCC1-RFP was 464

introduced into MT-GK lines. The roots of the T1 transgenetic lines were excised for imaging by a 465

Leica TCS SP5 confocal microscope. The DCC1-RFP signal was observed at 505–550 nm emission 466

after 561 nm excitation, whereas, the Mito-GFP signal was observed at 570–620 nm emission after 467

488 nm excitation. The merged signals of GFP and RFP showed yellow color. To detect the auxin 468

response pattern, approximately 60 calli cultured on SIM at different times were sampled to observe 469

the expression of DR5rev:GFP. The calli were cut into 1–2 mm sections along the longitudinal axis, 470

and the sections were viewed under a Leica TCS SP5 confocal microscope (Leica, Germany). The 471

GFP signal was observed at emission 505–550 nm after 488 nm excitation. 472

Phylogenetic Analysis 473

Phylogenetic analysis was used DCC1 (NP_568719.1) with its homologs in Camelina sativa 474

(XP_010441588.1), Brassica rapa (XP_010441588.1), Raphanus sativus (XP_018455194.1), 475

Gossypium hirsutum (XP_016755751.1), Ziziphus jujuba (XP_015882648.1), Malus domestica 476



17

(XP_008393058.1), Prunus persica (XP_007209569.1), Oryza officinalis (XP_015633461.1), Zea 477

mays (XP_008663715.1), Physcomitrella patens (XP_001777984.1), Populus trichocarpa 478

(XP_002322151.2), Vitis vinifera (XP_002283569.1), Triticum urartu (EMS60538.1), Microcystis 479

aeruginosa (WP_002792509.1), Arabidopsis thaliana (AT1G52590, NP_564611.1), Arabidopsis 480

thaliana (AT1G24095, NP_001185076.1), Caulobacter crescentus (NP_422377.1), Bacillus 481

halodurans (WP_010897025.1), and Pseudomonas aeruginosa (NP_249825.1). The analysis was 482

performed by MEGA 5.1 software. The protein sequences were downloaded from database of 483

National Center for Biotechnology Information (NCBI). 484

Thioredoxin Activity Assay 485

The construct pET28a-DCC1 was transferred into Rosetta competent cells. DCC1-His proteins 486

were induced by incubation in 1 mM IPTG at 22°C with shaking at 120 rpm for 16 h. The cell pellet 487

was resuspended in buffer (25 mM Tris, pH 7.5, 0.5 mM dithiothreitol [DTT]) (Motohashi et al., 488

2003). Protein purification was performed using Ni Sepharose 6 Fast Flow (GE Healthcare, 489

Piscataway, NJ, USA, catalog number 28-9355-97). Then, the proteins were dialyzed against buffer 490

(25 mM Tris, pH 7.5) to remove imidazole using Slide-A-Lyzer Dialysis Cassettes (ThermoFisher 491

Scientific, Rockford, IL, USA, catalog number 66810) for 24 h. Trx activity was measured using 492

the Thioredoxin Activity Fluorescent Assay Kit (Cayman Chemicals, Ann Arbor, MI, USA, catalog 493

number 11527). The fluorescein isothiocyanate-labeled insulin (FiTC-insulin) in the kit was used as 494

the substrate of DCC1. FiTC displays higher fluorescence after disulfide reduction (Montano et al., 495

2014). The reduction assay was performed by incubation with purified DCC1 protein (10 μg). 496

NADPH and TrxR were used to recycle the DCC1 Trx activity. The reaction mixture without DCC1 497

proteins was used as the control. The fluorescence intensity of each sample was recorded at 498

515–525 nm emission after excitation at 480–495 nm for 60 minutes using a BioTek Synergy™ 2 499

Multi-Mode Reader (BioTek, Winooski, VT, USA) at ambient room temperature. Three sets of 500

biological replicates were performed for each reaction. 501

Yeast Two-Hybrid Assay 502

The yeast two-hybrid assay was performed using the Matchmaker Gold Yeast Two-Hybrid 503

System (Clontech, Palo Alto, CA, USA, catalog number 630489) according to the manufacturer’s 504

instructions. The constructs DCC1-AD and CA2-BD were co-transferred into Y2H Gold competent 505

cells. Activation was observed at 3 days on selection plates (SD/ - Leu - Trp - His - Ade) with 506



18

X-α-gal. 507

Firefly Luciferase Complementation Assay 508

Firefly luciferase complementation assays were conducted as described previously (Li et al., 509

2014). The constructs DCC1-nLUC and CA2-cLUC were transformed into the leaf of N. 510

benthamiana for transient expression. Transfected leaves were sprayed with buffer (1 mM 511

D-luciferin sodium salt, 0.1% Triton X-100) 5 min before being imaged using the IVIS Lumina II 512

system (Caliper Life Sciences, Hopkinton, MA, USA). 513

Pull-Down Assay 514

For the pull-down assay, 10 μg CA2-GST protein was incubated with 10 μL 515

glutathione-Sepharose-4B beads (GE Healthcare; catalog number 17-0756-01) in blocking buffer 516

(140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1% w/v NP-40, 1 g BSA) 517

under agitation at 4°C for 2 h. 1 μg DCC1-His protein was added, and the mixture was incubated 518

for 2 h in binding buffer (140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1% 519

w/v NP-40). The beads were washed 10 times with washing buffer (400 mM NaCl, 2.7 mM KCl, 10 520

mM Na2HPO4, 1.8 mM KH2PO4, 0.1% w/v NP-40). Finally, 10% input and pull-down proteins 521

were separated by 12% SDS-PAGE and detected by immunoblotting using the antibodies anti-His, 522

diluted 1:3000 (Sigma, St Louis, MO, USA; catalog number H1029) or anti-GST, diluted 1:3000 523

(Sigma; catalog number G1160). 524

Co-Immunoprecipitation Assay 525

We used transgenic seedlings of 35S:DCC1-GFP and the F1 generation of 35S:DCC1-GFP × 526

35S:CA2-MYC for immunoprecipitation analyses. Proteins were extracted from 2 g seedlings with 527

extraction buffer (140 mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1 mM EDTA, 528

0.1% w/v NP-40, 5 mM DTT, 0.5 mM PMSF). Then, 60 μL beads were incubated with 10 μL 529

anti-GFP antibody with agitation for 2 h at 4°C. Then, supernatants were added and incubated with 530

agitation for 8 h at 4°C. After incubation, beads were washed 10 times with washing buffer (400 531

mM NaCl, 2.7 mM KCl, 10 mM Na2HPO4, 1.8 mM KH2PO4, 0.1 mM EDTA, 0.1% NP-40, 5 mM 532

DTT, 0.5 mM PMSF). Finally, 10% input and immunoprecipitation proteins were separated by 12% 533

SDS-PAGE and detected by immunoblotting using the antibodies anti-MYC, diluted 1:1000 (Sigma; 534

catalog number M4439) or anti-GFP, diluted 1:1000 (Roche, Mannheim, Germany; catalog number 535

11814460001). 536



19

Reduction of CA2 by DCC1 537

The reduction assay was performed as described previously with slight modifications (Yoshida et 538

al., 2015). The GST tag of the recombinant DCC1-GST proteins was cleaved by a thrombin (Sigma; 539

catalog number T9326). Purified CA2-His protein (1μM) was incubated with GST-cleaved DCC1 540

protein in the assay mixture containing 50 mM Tris-HCl (pH 7.5), 50 mM NaCl. DTT (0.3 mM) 541

was added to recycle DCC1 Trx activity. The mixture without DCC1 proteins was used as the 542

control. After incubation for 30 min at 25 °C, proteins were subjected to non-reducing (without 543

2-mercaptoethanol) or reducing (with 2-mercaptoethanol) SDS-PAGE followed by immunoblot 544

analysis using Anti-His antibody diluted 1:5000 (Sigma, catalog number H1029). 545

Mitochondrial Respiratory Complex I Activity Assay 546

Calli (0.1 g) of wild type (Col-0), dcc1, ca2, and dcc1ca2 cultured on SIM at 16 days were 547

collected, and then the mitochondria were isolated using a Plant Mitochondria Isolation Kit (Biohao, 548

Wuhan, China; catalog number P0045) according to the manufacturer’s instructions. Mitochondrial 549

respiratory complex Ⅰ activity was determined using 20 μg mitochondrial protein with a MitoCheck 550

Complex Ⅰ Activity Assay Kit (Cayman; catalog number 700930). The absorbance of all samples 551

was measured at 340 nm for 60 min using a plate reader. Complex Ⅰ activity was calculated from the 552

decrease in absorbance per minute. Standard errors were calculated from three sets of biological 553

replicates. 554

Chemical Treatments 555

Chemical reagents were added to the medium before transfer of calli, and calli were transferred to 556

new medium with fresh reagents every 6 days. Different concentrations of H2O2 (0.005‰, 0.01‰) 557

or GSH (100 μM, 300 μM and 600 μM) were added to the shoot regeneration system, and 10 μM 558

estradiol was added to induce the transcription of CAT3 to complement the phenotypes of dcc1, ca2, 559

and dcc1ca2. 560

DAB Staining Assay 561

Calli were incubated in DAB staining buffer (50 mM Tris, pH 7.6, 0.6 mg/mL DAB) at room 562

temperature in darkness, and then fixed in 70% v/v ethanol at room temperature. The calli were 563

observed under an Olympus DP72 microscope until the chlorophyll disappeared. The relative DAB 564

staining intensity was analyzed by Image J software. Three sets of biological replicates were 565

calculated and more than 30 calli were examined in each replicate. 566



20

Quantitative Real-Time PCR 567

Total RNA was isolated using TRI Reagent® (Sigma; catalog number T9424), and treated with 568

DNase Ι (Thermo Fisher Scientific, San Jose, CA, USA; catalog number EN0521). Then, cDNAs 569

were synthesized using M-MLV reverse transcriptase (Promega, Madison, WI, USA; catalog 570

number M1701). The qRT-PCR assays were conducted using a Bio-Rad CFX96 Real-Time PCR 571

Detection System (Bio-Rad, Hercules, CA, USA) in a 20-µL reaction volume with 45 cycles. The 572

cDNA levels were normalized against those of two housekeeping genes; TUBILIN2 (TUB2) and 573

ACTIN2 (ACT2). The relative expression level of each gene was standardized to TUB2 and 574

calculated using the comparative CT method (Schmittgen and Livak, 2008). Mean values were 575

calculated from three biological replicates. The sequences of primers used for qRT-PCR are listed in 576

Supplemental Table S4. 577

RNA Sequencing and Data Analyses 578

Three biological repeats of wild type (Col-0-A, Col-0-B and Col-0-C) and mutants dcc1 (dcc1-A, 579

dcc1-B and dcc1-C) were used for RNA sequencing. Total RNAs were isolated from the calli of 580

wild type Col-0 and dcc1 cultured on SIM at 16 days with TRI reagent (Sigma; catalog number 581

T9424). RNA was sequenced using the Illumina 2500 instrument in Gene Denovo Biotechnology 582

Co. (Guangzhou, China). The raw reads were aligned to the genome sequences of TAIR10 583

(www.arabidopsis.org) using Tophat2 software (version 2.0.3.12) (Kim et al., 2013). The gene 584

expression levels were measured in FPKM using Cufflinks software (Trapnell et al., 2014). 585

Statistical analyses were performed using the edgeR package (http://www.rproject.org/). 586

Differentially expressed genes were those with a fold change ≥ 2 and a false discovery rate (FDR) 587

<0.05 between the wild-type Col-0 and the mutant dcc1. A GO enrichment analysis was performed 588

in the Gene Ontology database (http://www.geneontology.org/) (Botstein et al., 2000). The RNA 589

sequencing data are available in the ArrayExpress database (www.ebi.ac.uk/arrayexpress) under the 590

accession number E-MTAB-5236. 591

Linkage Disequilibrium Analyses 592

Linkage disequilibrium analyses were performed using Genome Variation Server (GVS) (Carlson 593

et al., 2004) with DCC1 nucleotide sequences from 48 ecotypes of Arabidopsis. 594

Accession Numbers 595

Sequence data from this article can be found in the GenBank/EMBL data libraries under accession 596



21

numbers AT5G50100 (DCC1), AT1G47260 (CA2), , AT3G11260 (WOX5), AT3G03660 (WOX11), 597

AT5G17810 (WOX12), AT5G10510 (PLT3), AT5G57390 (PLT5), AT2G42430 (LBD16), 598

At2G42440 (LBD17), At2G45420 (LBD18), At3G58190 (LBD29), AT1G78080 (WIND1), 599

AT2G17950 (WUS), AT2G27250 (CLV3), AT1G62360 (STM). 600

Supplemental Data 601

Supplemental Figure S1. Identification of dcc1 mutant. 602

Supplemental Figure S2. Phenotypes of double mutant dcc1ca2 during shoot regeneration. 603

Supplemental Figure S3. Exogenous GSH promotes shoot regeneration. 604

Supplemental Figure S4. Transcript level of CAT3 in CAT3-overexpressing transgenic lines. 605

Supplemental Figure S5. Correlations among three biological repeats of RNA-seq analyses. 606

Supplemental Figure S6. Analyses of differentially expressed genes identified by RNA-seq were 607

confirmed by qRT-PCR. 608

Supplemental Figure S7. Shoot regeneration capacity of different Arabidopsis ecotypes. 609

Supplemental Table S1. Frequencies of shoot regeneration in the Trx mutants. 610

Supplemental Table S2. Up-regulated genes in dcc1 mutant as determined by RNA-seq analyses. 611

Supplemental Table S3. Down-regulated genes in dcc1 mutant as determined by RNA-seq 612

analyses. 613

Supplemental Table S4. Sequences of primers used in this study. 614

ACKNOWLEDGEMENTS 615

We thank all who generously provided plant materials in this research. We thank Dr. Min Ni 616

(Department of Plant Biology, University of Minnesota) for his critical reading of this manuscript. 617

618

Figure 1. Shoot regeneration is inhibited in dcc1 mutant. A to C, Callus morphology (A), 619

frequencies of shoot regeneration from calli (B), and number of shoots per callus (C) in wild type 620

(Col-0), dcc1, and dcc1 ProDCC1:DCC1 cultured on SIM at indicated times. D, Expression pattern 621

of DCC1 detected by in situ hybridization in calli of Col-0 at indicated times on SIM. E, Expression 622

pattern of DCC1 detected by GUS staining in calli of ProDCC1:DCC1-GUS transgenetic lines at 623

indicated times on SIM. S0 represents calli cultured on callus-induction medium (CIM) at 6 days 624

using roots as explants before transfer to SIM. S8, S12, S16, S20, S24 and S28 indicate calli 625

cultured on SIM at 8, 12, 16, 20, 24 and 28 days, respectively. Standard errors were calculated from 626



22

three sets of biological replicates and more than 100 calli were examined in each replicate. Scale 627

bars = 500 µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 628

Figure 2. DCC1 is a functional Trx localized in mitochondria. A, Models of DCC1 protein with a 629

mitochondria signal sequence predicted in UniProt database and a conserved DxxCxxC motif in a 630

function-unknown DUF393 domain analyzed in Pfam database. B, Alignment of the amino acid 631

sequences of different DCC family proteins. The DxxCxxC motif is a conserved signature sequence 632

for DCC family proteins in various species. The NCBI accession numbers of proteins in different 633

species are presented in Materials and Methods in detail. C, Phylogenetic analyses of DCC1 with its 634

homologs in various species. DCC1 shares high homology with several proteins in species, such as 635

Camelina sativa, Brassica rapa and Raphanus sativus. D, Insulin reduction by recombinant DCC1 636

proteins. Purified DCC1 proteins were subjected to a reduction assay by using fluorescein 637

isothiocyanate-labeled insulin (FiTC-insulin) as the substrate, which displayed higher fluorescence 638

after disulfide reduction. The assay mixture lacking recombinant DCC1 proteins served as the 639

control. Fluorescence intensity was recorded at 515-525 nm emission after 480-495 nm excitation 640

for 120 minutes in a fluorescent plate reader at room temperature. E, Subcellular localization of 641

DCC1. MT-GK is a well-established marker lines specially expressing GFP in mitochondria 642

(Mito-GFP). The construct 35S:DCC1-RFP was transformed into MT-GK lines. The T1 643

transgenetic lines roots were excised for imaging by a confocal microscope. The DCC1-RFP signal 644

(E1) was observed at 505–550 nm emission after 561 nm excitation, whereas, the Mito-GFP signal 645

(E2) was observed at 570–620 nm emission after 488 nm excitation. The merged signals of GFP 646

and RFP showed yellow color (E3), indicating DCC1 is localized in mitochondria. Scale bars = 20 647

µm. 648

Figure 3. DCC1 interacts with CA2. A, Interaction between DCC1 and CA2 in yeast two-hybrid 649

assay. Activation was observed at 3 days on selection plates (SD/ - Leu - Trp - His - Ade) with 650

X-α-gal. B, Interaction between DCC1 and CA2 in pull-down assay. GST-pull-down protein was 651

detected by immunoblotting using anti-His antibody. C, Interaction between DCC1 and CA2 in 652

firefly luciferase complementation assays in transiently transfected leaf of N. benthamiana. D, 653

Interaction between DCC1 and CA2 in co-immunoprecipitation assays. Immunoprecipitated protein 654

with anti-GFP was detected by immunoblotting using an anti-MYC antibody. 655

Figure 4. Loss-of-function of CA2 caused the decreased capacity of shoot regeneration. A to C, 656



23

Callus morphology (A), frequencies of shoot regeneration from calli (B) and number of shoots per 657

callus (C) in wild type (Col-0), ca2, and ca2 ProCA2:CA2 cultured on SIM at indicated times. D, 658

Expression pattern of CA2 detected by in situ hybridization in calli of Col-0 at indicated times on 659

SIM. E, Expression pattern of CA2 detected by GUS staining in calli of ProCA2:CA2-GUS 660

transgenetic lines at indicated times on SIM. S0 represents calli cultured on CIM at 6 days using 661

roots as explants before transfer to SIM. S8, S12, S16, S20, S24 and S28 indicate calli cultured on 662

SIM at 8, 12, 16, 20, 24 and 28 days, respectively. Standard errors were calculated from three sets 663

of biological replicates and more than 100 calli were examined in each replicate. Scale bars = 500 664

µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 665

Figure 5. DCC1 regulates complex I activity via CA2 protein. A and B, CA2 dimmer and oligomer 666

were reduced by DCC1. Purified CA2-His protein was incubated in the assay mixture with or 667

without DCC1 GST-cleaved protein (5 μM) for 30 min at room temperature and then subjected to 668

nonreducing (A) or reducing (B) SDS-PAGE followed by immunoblot analysis. DTT (0.3 mM) was 669

added to recycle DCC1 Trx activity. The position of the monomer, dimmer and oligomer of CA2 are 670

indicated. CA2 dimmer and oligomer showed significantly reduced levels when incubated with 671

DCC1 proteins (right lane). The reaction mixture without DCC1 proteins was used as the control 672

(left and middle lanes). C, Relative activity of mitochondrial respiratory complex I. Mitochondria 673

were isolated from calli (0.1 g) of wild type (Col-0), dcc1, ca2, and dcc1ca2 cultured on SIM at 16 674

days. 20 μg mitochondrial proteins were used to determine the Complex I activity. The absorbance 675

of all samples was measured at 340 nm for 60 min using a plate reader. Complex I activity was 676

calculated from the decrease in absorbance per minute. Functional loss of DCC1 or CA2 resulted in 677

the reduced activity of Complex I. D, Relative activity of complex I in calli of dcc1ca2 after 678

addition of recombinant CA2 or DCC1 proteins. Purified CA2-His proteins and DCC1-His proteins 679

were added to the assay mixture. Only both additions of DCC1 and CA2 proteins completely 680

rescued the reduced complex I activity. Significant difference, **p < 0.01 (Student’s one-tailed t 681

test). 682

Figure 6. Mutation of DCC1 or CA2 results in the increased ROS levels. A, Levels of ROS in calli 683

of Col-0, dcc1, ca2, and dcc1ca2 on CIM and SIM at indicated times by DAB staining. B, Relative 684

ROS staining intensity in calli of wild type (Col-0), dcc1, ca2, and dcc1ca2 on CIM and SIM at 685

indicated times. C3 and C6 indicate calli cultured on CIM at 3 and 6 days, respectively. S4, S8, S12 686



24

and S16 indicate calli cultured on SIM at 4, 8, 12 and 16 days, respectively. Standard errors were 687

calculated from three sets of biological replicates and more than 100 calli were examined in each 688

replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s one-tailed t test). 689

Figure 7. Treatment with exogenous ROS inhibits shoot regeneration. A to C, Callus morphology 690

(A), frequencies of shoot regeneration from calli (B) and number of shoots per callus (C) in wild 691

type (Col-0) after treatment with H2O2 at different concentrations during shoot regeneration. S12, 692

S16, S20, S24 and S28 indicate calli cultured on SIM at 12, 16, 20, 24 and 28 days, respectively. 693

Standard errors were calculated from three sets of biological replicates and more than 100 calli were 694

examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s 695

one-tailed t test). 696

Figure 8. Decreased ROS level rescues phenotypes of dcc1ca2 double mutant. A to C, Callus 697

morphology (A), frequencies of shoot regeneration from calli (B), and number of shoots per callus 698

(C) in wild type (Col-0), dcc1, ca2, and dcc1ca2 after treatment with GSH (600 μM) or 699

overexpression of CAT3 on SIM at 28 days. Glutathione (GSH) is a main endogenous antioxidant 700

responsible for ROS removal. CAT3 encodes a catalase, which catalyzes the breakdown of H2O2 701

into water and oxygen, thereby reducing the H2O2 level. pER8-CAT3 represents the over-expression 702

of CAT3 in dcc1, ca2, and dcc1ca2 background when induced with estradiol, respectively. Standard 703

errors were calculated from three sets of biological replicates and more than 100 calli were 704

examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 (Student’s 705

one-tailed t test). 706

Figure 9. Transcript levels of master genes involved in shoot regeneration. A and B, Transcript 707

levels of master genes for callus formation (A) and shoot meristem induction (B) during shoot 708

regeneration. C3 and C6 represent calli cultured on CIM at 3 and 6 days using roots as explants 709

before transfer to SIM. S4, S8, S12 and S16 indicate calli cultured on SIM at 4, 8, 12, 16 days, 710

respectively. Standard errors were calculated from three sets of biological replicates. Significant 711

difference, **p < 0.01 (Student’s one-tailed t test). 712

Figure 10. DCC1 regulates shoot regeneration through modulating multiple signaling by RNA-seq 713

analyses. A, Differential gene expression detected by edgeR. Two-fold change in gene transcript 714

levels between wild type Col-0 and mutant dcc1 with an adjusted P value (FDR) cutoff 0.05 was 715

considered as differential expression: 2332 genes were down-regulated and 689 genes were 716



25

up-regulated in dcc1 mutant. B, GO analyses of down-regulated genes in dcc1 mutant. C, Cluster 717

analysis of transcript levels of genes involved in auxin signaling, meristem initiation, and organ 718

formation. Col-0-A, Col-0-B, and Col-0-C were three repeats of Col-0. dcc1-A, dcc1-B, and dcc1-C 719

were three repeats of dcc1 mutant. D, Transcript levels of TAA1, YUC4, GH3.6, SAUR51, KNAT2, 720

CLV1, WOX1, and CUC1 in calli of Col-0, dcc1, and H2O2 (wild-type treated with 0.01‰ H2O2 721

during shoot regeneration) on SIM at 16 days, as determined by qRT-PCR. TUBULIN2 (TUB2) was 722

the reference gene. Significant difference, **p < 0.01 (Student’s one-tailed t test). E, Response 723

patterns of DR5rev:GFP in calli with or without H2O2 treatment on SIM at indicated times. S0, calli 724

cultured on CIM at 6 days using roots as explants before transfer to SIM. S4, S8, S12, S16, calli 725

cultured on SIM at 4, 8, 12 and 16 days, respectively. 726

Figure 11. DCC1 regulates the capacity of shoot regeneration among different Arabidopsis 727

ecotypes. A, Linkage disequilibrium analyses of DCC1 in 48 Arabidopsis ecotypes indicated five 728

critical SNPs (108, 147, 174, 175, 378, 481). B, Two haplotypes (Hap) of DCC1 was characterized 729

based on five SNPs of nucleotide sequences in Arabidopsis natural variants. C, Amino acid 730

sequence of Hap1 and Hap2. Two SNPs (SNP 175 and 481) resulted in amino acid mutation (I59V 731

and I161V). D and E, Shoot regeneration frequencies from calli (D) and number of shoots per callus 732

(E) in each haplotype group (n, number of genotypes belonging to each haplotype group). F, 733

Purified proteins were subjected to SDS-PAGE and stained by Coomassie Brilliant Blue R-250. 734

DCC1-WT from Col-0 was used as the control. DCC1-m175, DCC1-m481 and DCC1-m175/m481 735

were mutated according to Hap2 SNPs (SNP 175 and SNP 481). G, Insulin reduction assay by the 736

various proteins. Purified proteins were subjected to a reduction assay by using fluorescein 737

isothiocyanate-labeled insulin (FiTC-insulin) as the substrate, which displayed higher fluorescence 738

after disulfide reduction. The assay mixture lacking recombinant proteins served as the control. 739

Fluorescence intensity was recorded at 515-525 nm emission after 480-495 nm excitation for 120 740

minutes in a fluorescent plate reader at room temperature. H, Both SNP 175 and SNP 481 were 741

critical for interaction of DCC1 and CA2 by yeast two-hybrid assay. I, Frequencies of shoot 742

regeneration from calli of wild type (Col-0), dcc1, pDCC1:DCC1-dcc1, and 743

pDCC1:DCC1-m175-m481-dcc1 on SIM at 28 days. Significant difference, **p < 0.01; nsp > 0.05 744

(Student’s one-tailed t test). 745

Figure 12. ROS levels are associated with shoot regeneration capacity of different ecotypes in 746



26

Arabidopsis. A, DAB staining showing ROS levels in calli of different ecotypes of Hap1 cultured 747

on SIM at 16 days. B, DAB staining showing ROS levels in calli of different ecotypes of Hap2 748

cultured on SIM at 16 days. C, Shoot regeneration frequencies from calli of different ecotypes 749

cultured on SIM at 28 days. D, Number of shoots per callus of different ecotypes cultured on SIM at 750

28 days. E, Relative staining intensity of ROS in calli of different ecotypes cultured on SIM at 16 751

days. Standard errors were calculated from three sets of biological replicates and more than 100 752

calli were examined in each replicate. Scale bars = 500 µm. Significant difference, **p < 0.01 753

(Student’s one-tailed t test). 754

755

LITERATURE CITED 756

Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis 757 interactome map. Science 333: 601 758

Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay 759 between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 760 376-391 761

Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot J-P, Manieri W, Schürmann P, 762 Droux M, et al (2004) Thioredoxin links redox to the regulation of fundamental processes of plant 763 mitochondria. Proc Natl Acad Sci USA 101: 2642-2647 764

Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis 765 meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 766 106: 3615-3620 767

Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710 768 Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, 769

et al (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29 770 Braun H-P, Binder S, Brennicke A, Eubel H, Fernie AR, Finkemeier I, Klodmann J, König A-C, Kühn K, Meyer 771

E (2014) The life of plant mitochondrial complex I. Mitochondrion 19: 295-313 772 Carlson CS, Eberle MA, Rieder MJ, Yi Q, Kruglyak L, Nickerson DA (2004) Selecting a maximally informative set 773

of single-nucleotide polymorphisms for association analyses using linkage disequilibrium. Am J Hum Genet 774 74: 106-120 775

Challa KR, Aggarwal P, Nath U (2016) Activation of YUCCA5 by the transcription factor TCP4 integrates 776 developmental and environmental signals to promote hypocotyl elongation in Arabidopsis. Plant Cell 2016: 777 2016 778

Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, et al (2013) Pattern of auxin 779 and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by 780 AUXIN RESPONSE FACTOR3. Plant Physiol 161: 240-251 781

Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxid Redox Sign 21: 1305-1326 782 Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox-and reactive oxygen species-dependent signaling into and out 783

of the photosynthesizing chloroplast. Plant Physiol 171: 1541-1550 784 Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11: 785

329-334 786



27

Dröse S, Brandt U, Wittig I (2014) Mitochondrial respiratory chain complexes as sources and targets of thiol-based 787 redox-regulation. BBA-Proteins Proteom 1844: 1344-1354 788

Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. 789 Trends Plant Sci 16: 597-606 790

Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus 791 formation in Arabidopsis regeneration. Cell Res 22: 1169-1180 792

Galkin A, Meyer B, Wittig I, Karas M, Schägger H, Vinogradov A, Brandt U (2008) Identification of the 793 mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of 794 respiratory complex I. J Biol Chem 283: 20907-20913 795

Gelhaye E, Rouhier N, Navrot N, Jacquot J (2005) The plant thioredoxin system. Cell Mol Life Sci 62: 24-35 796 Ginalski K, Kinch L, Rychlewski L, Grishin NV (2004) DCC proteins: a novel family of thiol-disulfide 797

oxidoreductases. Trends Biochem Sci 29: 339-342 798 Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo 799

assembly of the Arabidopsis shoot meristem. Development 134: 3539-3548 800 Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol 801

Biol 49: 373-385 802 Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen 803

species in cellular signaling and stress response in plants. Plant Physiol 171: 1551-1559 804 Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. 805

Development 143: 1442-1451 806 Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, et al 807

(2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21: 808 508-514 809

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major 810 determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347 811

Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, 812 Meyerowitz EM, Scheres B, et al (2015) PLETHORA genes control regeneration by a two-step mechanism. 813 Curr Biol 25: 1017-1030 814

Karimi M, Inzé D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends 815 Plant Sci 7: 193-195 816

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of 817 transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36 818

Kimura S, Waszczak C, Hunter K, Wrzaczek M (2017) Bound by fate: the role of reactive oxygen species in 819 receptor-like kinase signaling. Plant Cell 29: 638-654 820

Lall S, Nettleton D, DeCook R, Che P, Howell SH (2004) Quantitative trait loci associated with adventitious shoot 821 formation in tissue culture and the program of shoot development in Arabidopsis. Genetics 167: 1883-1892 822

Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011a) DNA methylation and histone modifications 823 regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. 824 PLoS Genet 7: e1002243 825

Li XR, Li HJ, Yuan L, Liu M, Shi DQ, Liu J, Yang WC (2014) Arabidopsis DAYU/ABERRANT PEROXISOME 826 MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen 827 maturation and germination in planta. Plant Cell 26: 619-635 828

Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, et al (2011b) Natural variation in GS5 829 plays an important role in regulating grain size and yield in rice. Nat Genet 43: 1266-1269 830

Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate 831



28

transition during de novo root organogenesis in Arabidopsis. Plant Cell 26: 1081-1093 832 Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JH (2014) Transcriptional control of ROS homeostasis by 833

KUODA1 regulates cell expansion during leaf development. Nat Commun 5: 3767 834 Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 66: 75-87 835 Lucero LE, Uberti-Manassero NG, Arce AL, Colombatti F, Alemano SG, Gonzalez DH (2015) TCP15 modulates 836

cytokinin and auxin responses during gynoecium development in Arabidopsis. Plant J 84: 267-282 837 Mangano S, Juárez SPD, Estevez JM (2016) ROS regulation of polar growth in plant cells. Plant Physiol 171: 838

1593-1605 839 Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (2010) A membrane-associated thioredoxin required for 840

plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci 841 USA 107: 3900-3905 842

Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, Tang YY, Zhang XS (2017) Type-B 843 ARABIDOPSIS RESPONSE REGULATORs Is critical to the specification of shoot stem cell niche by dual 844 regulation of WUSCHEL. Plant Cell 29: 1357-1372 845

Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86: 419-433 846 Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in 847

Arabidopsis. Nature 441: 947-952 848 Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR (2010) 849

Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins 850 ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 154: 1492-1504 851

Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in 852 plants: the first 30 years. J Proteomics 72: 452-474 853

Montano SJ, Lu J, Gustafsson TN, Holmgren A (2014) Activity assays of mammalian thioredoxin and thioredoxin 854 reductase: fluorescent disulfide substrates, mechanisms, and use with tissue samples. Anal Biochem 449: 855 139-146 856

Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T (2003) Chloroplast cyclophilin is a target 857 protein of thioredoxin. J Biol Chem 278: 31848-31852 858

Motte H, Vercauteren A, Depuydt S, Landschoot S, Geelen D, Werbrouck S, Goormachtig S, Vuylsteke M, 859 Vereecke D (2014) Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN 860 KINASE1 as an essential Arabidopsis shoot regeneration gene. Proc Natl Acad Sci USA 111: 8305-8310 861

Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in 862 Arabidopsis and other plants. Plant J 51: 1126-1136 863

Rogers H, Munné-Bosch S (2016) Production and scavenging of reactive oxygen species and redox signaling during 864 leaf and flower senescence: similar but different. Plant Physiol 171: 1560-1568 865

Rouhier N, Cerveau D, Couturier J, Reichheld JP, Rey P (2015) Involvement of thiol-based mechanisms in plant 866 development. BBA-Gen Subjects 1850: 1479-1496 867

Sandalio L, Romero-Puertas M (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and 868 RNS signalling networks. Ann Bot 116: 475-485 869

Schiantarelli E, De la Peña A, Candela M (2001) Use of recombinant inbred lines (RILs) to identify, locate and map 870 major genes and quantitative trait loci involved with in vitro regeneration ability in Arabidopsis thaliana. 871 Theor Appl Genet 102: 335-341 872

Schippers JH, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. 873 Curr Opin Plant Biol 29: 121-128 874

Schmidt R, Schippers JH (2015) ROS-mediated redox signaling during cell differentiation in plants. BBA-Gen 875 Subjects 1850: 1497-1508 876



29

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 877 1101-1108 878

Scofield S, Dewitte W, Murray JAH (2007) The KNOX gene SHOOT MERISTEMLESS is required for the 879 development of reproductive meristematic tissues in Arabidopsis. Plant J 50: 767-781 880

Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements 881 for spatial regulation are located intragenically. Plant Cell 9: 355-365 882

Soto D, Cordoba JP, Villarreal F, Bartoli C, Schmitz J, Maurino VG, Braun HP, Pagnussat GC, Zabaleta E (2015) 883 Functional characterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I 884 in Arabidopsis thaliana. Plant J 83: 831-844 885

Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of 886 an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17: 616-627 887

Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for 888 embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59: 448-460 889

Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root 890 development pathway. Dev Cell 18: 463-471 891

Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity 892 requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321: 952-956 893

Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2014) 894 Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat 895 Protoco 7: 562-578 896

Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to 897 differentiation in the root. Cell 143: 606-616 898

van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 899 10: 2009-2010 900

Velázquez I, Valencia S, López-Lera A, de la Peña A, Candela M (2004) Analysis of natural allelic variation in in 901 vitro organogenesis of Arabidopsis thaliana. Euphytica 137: 73-79 902

Viola IL, Güttlein LN, Gonzalez DH (2013) Redox modulation of plant developmental regulators from the class I 903 TCP transcription factor family. Plant Physiol 162: 1434-1447 904

Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to 905 drought tolerance in maize seedlings. Nat Genet 48: 1233-1241 906

Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops - production, perception, regulation. Curr Opin 907 Plant Biol 16: 575-582 908

Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is 909 critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26: 2007-2023 910

Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006) A molecular framework for plant regeneration. 911 Science 311: 385-388 912

Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in 913 plant mitochondria. Plant Cell Physiol 54: 875-892 914

Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in 915 chloroplasts. J Biol Chem 290: 14278-14288 916

Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-Loop NTPase regulates quiescent center cell division 917 and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12: 918 e1006175 919

Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F (2015) Oxidative post-translational 920 modifications of cysteine residues in plant signal transduction. J Exp Bot 66: 2923-2934 921



30

Zhang TQ, Lian H, Zhou CM, Xu L, Jiao Y, Wang JW (2017) A Two-Step Model for de novo Activation of 922 WUSCHEL during Plant Shoot Regeneration. The Plant Cell 29: 1073-1087 923

Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Bio 61: 49-64 924 Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis 925

CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated 926 signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27: 1445-1460 927

928



























Parsed CitationsArabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science333: 601

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linkedthioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 376-391


Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot J-P, Manieri W, Schürmann P, Droux M, et al (2004)Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101: 2642-2647


Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristemdevelopment by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106: 3615-3620


Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al (2000) GeneOntology: tool for the unification of biology. Nat Genet 25: 25-29


Braun H-P, Binder S, Brennicke A, Eubel H, Fernie AR, Finkemeier I, Klodmann J, König A-C, Kühn K, Meyer E (2014) The life ofplant mitochondrial complex I. Mitochondrion 19: 295-313


Carlson CS, Eberle MA, Rieder MJ, Yi Q, Kruglyak L, Nickerson DA (2004) Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium. Am J Hum Genet 74: 106-120


Challa KR, Aggarwal P, Nath U (2016) Activation of YUCCA5 by the transcription factor TCP4 integrates developmental andenvironmental signals to promote hypocotyl elongation in Arabidopsis. Plant Cell 2016: 2016


Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, et al (2013) Pattern of auxin and cytokininresponses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3.Plant Physiol 161: 240-251


Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxid Redox Sign 21: 1305-1326Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox-and reactive oxygen species-dependent signaling into and out of thephotosynthesizing chloroplast. Plant Physiol 171: 1541-1550


Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11: 329-334Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Dröse S, Brandt U, Wittig I (2014) Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation. BBA-Proteins Proteom 1844: 1344-1354 www.plantphysiol.orgon July 21, 2017 - Published by Downloaded from

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http://search.crossref.org/?page=1&rows=2&q=Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Arabidopsis&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Evidence for network evolution in an Arabidopsis interactome map.&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=Evidence for network evolution in an Arabidopsis interactome map.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Arabidopsis&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bashandy T%2C Guilleminot J%2C Vernoux T%2C Caparros%2DRuiz D%2C Ljung K%2C Meyer Y%2C Reichheld JP %282010%29 Interplay between the NADP%2Dlinked thioredoxin and glutathione systems in Arabidopsis auxin signaling%2E Plant Cell 22%3A 376%2D391&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22: 376-391

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bashandy&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling&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=Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bashandy&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Balmer Y%2C Vensel WH%2C Tanaka CK%2C Hurkman WJ%2C Gelhaye E%2C Rouhier N%2C Jacquot J%2DP%2C Manieri W%2C Sch�rmann P%2C Droux M%2C et al %282004%29 Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria%2E Proc Natl Acad Sci USA 101%3A 2642%2D2647&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot J-P, Manieri W, Sch�rmann P, Droux M, et al (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101: 2642-2647

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Balmer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria&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=Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Balmer&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Benitez%2DAlfonso Y%2C Cilia M%2C San Roman A%2C Thomas C%2C Maule A%2C Hearn S%2C Jackson D %282009%29 Control of Arabidopsis meristem development by thioredoxin%2Ddependent regulation of intercellular transport%2E Proc Natl Acad Sci USA 106%3A 3615%2D3620&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106: 3615-3620

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Benitez-Alfonso&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport&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 Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Benitez-Alfonso&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Birnbaum KD%2C Alvarado AS %282008%29 Slicing across kingdoms%3A regeneration in plants and animals%2E Cell 132%3A 697%2D710&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132: 697-710

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Birnbaum&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Slicing across kingdoms: regeneration in plants and animals&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=Slicing across kingdoms: regeneration in plants and animals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Birnbaum&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ashburner M%2C Ball CA%2C Blake JA%2C Botstein D%2C Butler H%2C Cherry JM%2C Davis AP%2C Dolinski K%2C Dwight SS%2C Eppig JT%2C et al %282000%29 Gene Ontology%3A tool for the unification of biology%2E Nat Genet 25%3A 25%2D29&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ashburner&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Gene Ontology: tool for the unification of biology&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 Ontology: tool for the unification of biology&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ashburner&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Braun H%2DP%2C Binder S%2C Brennicke A%2C Eubel H%2C Fernie AR%2C Finkemeier I%2C Klodmann J%2C K�nig A%2DC%2C K�hn K%2C Meyer E %282014%29 The life of plant mitochondrial complex I%2E Mitochondrion 19%3A 295%2D313&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Braun H-P, Binder S, Brennicke A, Eubel H, Fernie AR, Finkemeier I, Klodmann J, K�nig A-C, K�hn K, Meyer E (2014) The life of plant mitochondrial complex I. Mitochondrion 19: 295-313

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Braun&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The life of plant mitochondrial complex I&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 life of plant mitochondrial complex I&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Braun&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Carlson CS%2C Eberle MA%2C Rieder MJ%2C Yi Q%2C Kruglyak L%2C Nickerson DA %282004%29 Selecting a maximally informative set of single%2Dnucleotide polymorphisms for association analyses using linkage disequilibrium%2E Am J Hum Genet 74%3A 106%2D120&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Carlson CS, Eberle MA, Rieder MJ, Yi Q, Kruglyak L, Nickerson DA (2004) Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium. Am J Hum Genet 74: 106-120

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Carlson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium&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=Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Carlson&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Challa KR%2C Aggarwal P%2C Nath U %282016%29 Activation of YUCCA5 by the transcription factor TCP4 integrates developmental and environmental signals to promote hypocotyl elongation in Arabidopsis%2E Plant Cell 2016%3A 2016&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Challa KR, Aggarwal P, Nath U (2016) Activation of YUCCA5 by the transcription factor TCP4 integrates developmental and environmental signals to promote hypocotyl elongation in Arabidopsis. Plant Cell 2016: 2016

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Challa&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Activation of YUCCA5 by the transcription factor TCP4 integrates developmental and environmental signals to promote hypocotyl elongation 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=Activation of YUCCA5 by the transcription factor TCP4 integrates developmental and environmental signals to promote hypocotyl elongation in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Challa&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cheng ZJ%2C Wang L%2C Sun W%2C Zhang Y%2C Zhou C%2C Su YH%2C Li W%2C Sun TT%2C Zhao XY%2C Li XG%2C et al %282013%29 Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3%2E Plant Physiol 161%3A 240%2D251&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, et al (2013) Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol 161: 240-251

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Cheng&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3&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=Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cheng&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Considine MJ%2C Foyer CH %282014%29 Redox regulation of plant development%2E Antioxid Redox Sign 21%3A 1305%2D1326&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Considine MJ, Foyer CH (2014) Redox regulation of plant development. Antioxid Redox Sign 21: 1305-1326

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Considine&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Redox regulation of plant 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=Redox regulation of plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Considine&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dietz KJ%2C Turkan I%2C Krieger%2DLiszkay A %282016%29 Redox%2Dand reactive oxygen species%2Ddependent signaling into and out of the photosynthesizing chloroplast%2E Plant Physiol 171%3A 1541%2D1550&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox-and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171: 1541-1550

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Dietz&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Redox-and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast&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=Redox-and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dietz&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Dos Santos CV%2C Rey P %282006%29 Plant thioredoxins are key actors in the oxidative stress response%2E Trends Plant Sci 11%3A 329%2D334&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11: 329-334

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Dos&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant thioredoxins are key actors in the oxidative stress response&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 thioredoxins are key actors in the oxidative stress response&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dos&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1



Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends PlantSci 16: 597-606


Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation inArabidopsis regeneration. Cell Res 22: 1169-1180


Galkin A, Meyer B, Wittig I, Karas M, Schägger H, Vinogradov A, Brandt U (2008) Identification of the mitochondrial ND3 subunit asa structural component involved in the active/deactive enzyme transition of respiratory complex I. J Biol Chem 283: 20907-20913


Gelhaye E, Rouhier N, Navrot N, Jacquot J (2005) The plant thioredoxin system. Cell Mol Life Sci 62: 24-35Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ginalski K, Kinch L, Rychlewski L, Grishin NV (2004) DCC proteins: a novel family of thiol-disulfide oxidoreductases. TrendsBiochem Sci 29: 339-342


Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of theArabidopsis shoot meristem. Development 134: 3539-3548


Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49: 373-385


Huang S, Van Aken O, Schwarzländer M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellularsignaling and stress response in plants. Plant Physiol 171: 1551-1559


Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143:1442-1451


Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, et al (2011) The AP2/ERFtranscription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21: 508-514


Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of naturalvariation in Arabidopsis flowering time. Science 290: 344-347


Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, etal (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25: 1017-1030


Karimi M, Inzé D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193-195



http://www.ncbi.nlm.nih.gov/pubmed?term=Dr�se S%2C Brandt U%2C Wittig I %282014%29 Mitochondrial respiratory chain complexes as sources and targets of thiol%2Dbased redox%2Dregulation%2E BBA%2DProteins Proteom 1844%3A 1344%2D1354&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Dr�se S, Brandt U, Wittig I (2014) Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation. BBA-Proteins Proteom 1844: 1344-1354

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Dr�se&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation&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=Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Dr�se&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Duclercq J%2C Sangwan%2DNorreel B%2C Catterou M%2C Sangwan RS %282011%29 De novo shoot organogenesis%3A from art to science%2E Trends Plant Sci 16%3A 597%2D606&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci 16: 597-606

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Duclercq&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=De novo shoot organogenesis: from art to science&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=De novo shoot organogenesis: from art to science&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Duclercq&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fan M%2C Xu C%2C Xu K%2C Hu Y %282012%29 LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration%2E Cell Res 22%3A 1169%2D1180&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fan M, Xu C, Xu K, Hu Y (2012) LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res 22: 1169-1180

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration&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=LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fan&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Galkin A%2C Meyer B%2C Wittig I%2C Karas M%2C Sch�gger H%2C Vinogradov A%2C Brandt U %282008%29 Identification of the mitochondrial ND3 subunit as a structural component involved in the active%2Fdeactive enzyme transition of respiratory complex I%2E J Biol Chem 283%3A 20907%2D20913&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Galkin A, Meyer B, Wittig I, Karas M, Sch�gger H, Vinogradov A, Brandt U (2008) Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I. J Biol Chem 283: 20907-20913

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Galkin&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I&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=Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Galkin&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gelhaye E%2C Rouhier N%2C Navrot N%2C Jacquot J %282005%29 The plant thioredoxin system%2E Cell Mol Life Sci 62%3A 24%2D35&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gelhaye E, Rouhier N, Navrot N, Jacquot J (2005) The plant thioredoxin system. Cell Mol Life Sci 62: 24-35

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gelhaye&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The plant thioredoxin system&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 plant thioredoxin system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gelhaye&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ginalski K%2C Kinch L%2C Rychlewski L%2C Grishin NV %282004%29 DCC proteins%3A a novel family of thiol%2Ddisulfide oxidoreductases%2E Trends Biochem Sci 29%3A 339%2D342&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ginalski K, Kinch L, Rychlewski L, Grishin NV (2004) DCC proteins: a novel family of thiol-disulfide oxidoreductases. Trends Biochem Sci 29: 339-342

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ginalski&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=DCC proteins: a novel family of thiol-disulfide oxidoreductases&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=DCC proteins: a novel family of thiol-disulfide oxidoreductases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ginalski&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gordon SP%2C Heisler MG%2C Reddy GV%2C Ohno C%2C Das P%2C Meyerowitz EM %282007%29 Pattern formation during de novo assembly of the Arabidopsis shoot meristem%2E Development 134%3A 3539%2D3548&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134: 3539-3548

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gordon&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Pattern formation during de novo assembly of the Arabidopsis shoot meristem&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=Pattern formation during de novo assembly of the Arabidopsis shoot meristem&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gordon&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Hagen G%2C Guilfoyle T %282002%29 Auxin%2Dresponsive gene expression%3A genes%2C promoters and regulatory factors%2E Plant Mol Biol 49%3A 373%2D385&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49: 373-385

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hagen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin-responsive gene expression: genes, promoters and regulatory 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=Auxin-responsive gene expression: genes, promoters and regulatory factors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hagen&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Huang S%2C Van Aken O%2C Schwarzl�nder M%2C Belt K%2C Millar AH %282016%29 The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants%2E Plant Physiol 171%3A 1551%2D1559&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Huang S, Van Aken O, Schwarzl�nder M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol 171: 1551-1559

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Huang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The roles of mitochondrial reactive oxygen species in cellular signaling and stress response 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=The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Huang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ikeuchi M%2C Ogawa Y%2C Iwase A%2C Sugimoto K %282016%29 Plant regeneration%3A cellular origins and molecular mechanisms%2E Development 143%3A 1442%2D1451&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143: 1442-1451

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ikeuchi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant regeneration: cellular origins and molecular 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 regeneration: cellular origins and molecular mechanisms&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ikeuchi&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Iwase A%2C Mitsuda N%2C Koyama T%2C Hiratsu K%2C Kojima M%2C Arai T%2C Inoue Y%2C Seki M%2C Sakakibara H%2C Sugimoto K%2C et al %282011%29 The AP2%2FERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis%2E Curr Biol 21%3A 508%2D514&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, et al (2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21: 508-514

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=The AP2/ERF transcription factor WIND1 controls cell dedifferentiation 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 AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Iwase&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Johanson U%2C West J%2C Lister C%2C Michaels S%2C Amasino R%2C Dean C %282000%29 Molecular analysis of FRIGIDA%2C a major determinant of natural variation in Arabidopsis flowering time%2E Science 290%3A 344%2D347&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Johanson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time&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 analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Johanson&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kareem A%2C Durgaprasad K%2C Sugimoto K%2C Du Y%2C Pulianmackal AJ%2C Trivedi ZB%2C Abhayadev PV%2C Pinon V%2C Meyerowitz EM%2C Scheres B%2C et al %282015%29 PLETHORA genes control regeneration by a two%2Dstep mechanism%2E Curr Biol 25%3A 1017%2D1030&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev PV, Pinon V, Meyerowitz EM, Scheres B, et al (2015) PLETHORA genes control regeneration by a two-step mechanism. Curr Biol 25: 1017-1030

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kareem&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=PLETHORA genes control regeneration by a two-step mechanism&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=PLETHORA genes control regeneration by a two-step mechanism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kareem&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Karimi M%2C Inz� D%2C Depicker A %282002%29 GATEWAYTM vectors for Agrobacterium%2Dmediated plant transformation%2E Trends Plant Sci 7%3A 193%2D195&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Karimi M, Inz� D, Depicker A (2002) GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Karimi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=GATEWAYTM vectors for Agrobacterium-mediated plant 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=GATEWAYTM vectors for Agrobacterium-mediated plant transformation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Karimi&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1


Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in thepresence of insertions, deletions and gene fusions. Genome Biol 14: R36


Kimura S, Waszczak C, Hunter K, Wrzaczek M (2017) Bound by fate: the role of reactive oxygen species in receptor-like kinasesignaling. Plant Cell 29: 638-654


Lall S, Nettleton D, DeCook R, Che P, Howell SH (2004) Quantitative trait loci associated with adventitious shoot formation intissue culture and the program of shoot development in Arabidopsis. Genetics 167: 1883-1892


Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011a) DNA methylation and histone modifications regulate de novoshoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7: e1002243


Li XR, Li HJ, Yuan L, Liu M, Shi DQ, Liu J, Yang WC (2014) Arabidopsis DAYU/ABERRANT PEROXISOME MORPHOLOGY9 is a keyregulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta. Plant Cell 26: 619-635


Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, et al (2011b) Natural variation in GS5 plays an important rolein regulating grain size and yield in rice. Nat Genet 43: 1266-1269


Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during denovo root organogenesis in Arabidopsis. Plant Cell 26: 1081-1093


Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JH (2014) Transcriptional control of ROS homeostasis by KUODA1regulates cell expansion during leaf development. Nat Commun 5: 3767


Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 66: 75-87Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lucero LE, Uberti-Manassero NG, Arce AL, Colombatti F, Alemano SG, Gonzalez DH (2015) TCP15 modulates cytokinin and auxinresponses during gynoecium development in Arabidopsis. Plant J 84: 267-282


Mangano S, Juárez SPD, Estevez JM (2016) ROS regulation of polar growth in plant cells. Plant Physiol 171: 1593-1605Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (2010) A membrane-associated thioredoxin required for plant growthmoves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci USA 107: 3900-3905


Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, Tang YY, Zhang XS (2017) Type-B ARABIDOPSIS RESPONSEREGULATORs Is critical to the specification of shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29: 1357-1372


Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86: 419-433Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title www.plantphysiol.orgon July 21, 2017 - Published by Downloaded from


http://www.ncbi.nlm.nih.gov/pubmed?term=Kim D%2C Pertea G%2C Trapnell C%2C Pimentel H%2C Kelley R%2C Salzberg SL %282013%29 TopHat2%3A accurate alignment of transcriptomes in the presence of insertions%2C deletions and gene fusions%2E Genome Biol 14%3A R36&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36

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=TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.&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=TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.&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=Kimura S%2C Waszczak C%2C Hunter K%2C Wrzaczek M %282017%29 Bound by fate%3A the role of reactive oxygen species in receptor%2Dlike kinase signaling%2E Plant Cell 29%3A 638%2D654&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kimura S, Waszczak C, Hunter K, Wrzaczek M (2017) Bound by fate: the role of reactive oxygen species in receptor-like kinase signaling. Plant Cell 29: 638-654

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kimura&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Bound by fate: the role of reactive oxygen species in receptor-like kinase signaling&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=Bound by fate: the role of reactive oxygen species in receptor-like kinase signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kimura&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lall S%2C Nettleton D%2C DeCook R%2C Che P%2C Howell SH %282004%29 Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in Arabidopsis%2E Genetics 167%3A 1883%2D1892&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lall S, Nettleton D, DeCook R, Che P, Howell SH (2004) Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in Arabidopsis. Genetics 167: 1883-1892

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lall&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development 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=Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lall&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Li W%2C Liu H%2C Cheng ZJ%2C Su YH%2C Han HN%2C Zhang Y%2C Zhang XS %282011a%29 DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling%2E PLoS Genet 7%3A e1002243&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011a) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7: e1002243

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Li&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling.&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=DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Li XR%2C Li HJ%2C Yuan L%2C Liu M%2C Shi DQ%2C Liu J%2C Yang WC %282014%29 Arabidopsis DAYU%2FABERRANT PEROXISOME MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta%2E Plant Cell 26%3A 619%2D635&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li XR, Li HJ, Yuan L, Liu M, Shi DQ, Liu J, Yang WC (2014) Arabidopsis DAYU/ABERRANT PEROXISOME MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta. Plant Cell 26: 619-635


http://scholar.google.com/scholar?as_q=Arabidopsis DAYU/ABERRANT PEROXISOME MORPHOLOGY9 is a key regulator of peroxisome biogenesis and plays critical roles during pollen maturation and germination in planta&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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Li Y%2C Fan C%2C Xing Y%2C Jiang Y%2C Luo L%2C Sun L%2C Shao D%2C Xu C%2C Li X%2C Xiao J%2C et al %282011b%29 Natural variation in GS5 plays an important role in regulating grain size and yield in rice%2E Nat Genet 43%3A 1266%2D1269&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, et al (2011b) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43: 1266-1269


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http://search.crossref.org/?page=1&rows=2&q=Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26: 1081-1093

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http://search.crossref.org/?page=1&rows=2&q=Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JH (2014) Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat Commun 5: 3767

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf 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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lu J%2C Holmgren A %282014%29 The thioredoxin antioxidant system%2E Free Radic Biol Med 66%3A 75%2D87&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lu J, Holmgren A (2014) The thioredoxin antioxidant system. Free Radic Biol Med 66: 75-87

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The thioredoxin antioxidant system&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 thioredoxin antioxidant system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lu&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lucero LE%2C Uberti%2DManassero NG%2C Arce AL%2C Colombatti F%2C Alemano SG%2C Gonzalez DH %282015%29 TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis%2E Plant J 84%3A 267%2D282&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lucero LE, Uberti-Manassero NG, Arce AL, Colombatti F, Alemano SG, Gonzalez DH (2015) TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis. Plant J 84: 267-282

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mangano S%2C Ju�rez SPD%2C Estevez JM %282016%29 ROS regulation of polar growth in plant cells%2E Plant Physiol 171%3A 1593%2D1605&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mangano S, Ju�rez SPD, Estevez JM (2016) ROS regulation of polar growth in plant cells. Plant Physiol 171: 1593-1605

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http://scholar.google.com/scholar?as_q=ROS regulation of polar growth in plant cells&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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Meng L%2C Wong JH%2C Feldman LJ%2C Lemaux PG%2C Buchanan BB %282010%29 A membrane%2Dassociated thioredoxin required for plant growth moves from cell to cell%2C suggestive of a role in intercellular communication%2E Proc Natl Acad Sci USA 107%3A 3900%2D3905&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (2010) A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci USA 107: 3900-3905

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http://scholar.google.com/scholar?as_q=A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication&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 membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Meng&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Meng WJ%2C Cheng ZJ%2C Sang YL%2C Zhang MM%2C Rong XF%2C Wang ZW%2C Tang YY%2C Zhang XS %282017%29 Type%2DB ARABIDOPSIS RESPONSE REGULATORs Is critical to the specification of shoot stem cell niche by dual regulation of WUSCHEL%2E Plant Cell 29%3A 1357%2D1372&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, Tang YY, Zhang XS (2017) Type-B ARABIDOPSIS RESPONSE REGULATORs Is critical to the specification of shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29: 1357-1372

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http://scholar.google.com/scholar?as_q=Type-B ARABIDOPSIS RESPONSE REGULATORs Is critical to the specification of shoot stem cell niche by dual regulation of WUSCHEL&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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Meyer Y%2C Reichheld JP%2C Vignols F %282005%29 Thioredoxins in Arabidopsis and other plants%2E Photosynth Res 86%3A 419%2D433&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86: 419-433

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Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947-952


Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR (2010) Arabidopsis basicleucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantlyrequired for anther development. Plant Physiol 154: 1492-1504


Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30years. J Proteomics 72: 452-474


Montano SJ, Lu J, Gustafsson TN, Holmgren A (2014) Activity assays of mammalian thioredoxin and thioredoxin reductase:fluorescent disulfide substrates, mechanisms, and use with tissue samples. Anal Biochem 449: 139-146


Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T (2003) Chloroplast cyclophilin is a target protein ofthioredoxin. J Biol Chem 278: 31848-31852


Motte H, Vercauteren A, Depuydt S, Landschoot S, Geelen D, Werbrouck S, Goormachtig S, Vuylsteke M, Vereecke D (2014)Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN KINASE1 as an essential Arabidopsis shootregeneration gene. Proc Natl Acad Sci USA 111: 8305-8310


Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis andother plants. Plant J 51: 1126-1136


Rogers H, Munné-Bosch S (2016) Production and scavenging of reactive oxygen species and redox signaling during leaf andflower senescence: similar but different. Plant Physiol 171: 1560-1568


Rouhier N, Cerveau D, Couturier J, Reichheld JP, Rey P (2015) Involvement of thiol-based mechanisms in plant development.BBA-Gen Subjects 1850: 1479-1496


Sandalio L, Romero-Puertas M (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNSsignalling networks. Ann Bot 116: 475-485


Schiantarelli E, De la Peña A, Candela M (2001) Use of recombinant inbred lines (RILs) to identify, locate and map major genes andquantitative trait loci involved with in vitro regeneration ability in Arabidopsis thaliana. Theor Appl Genet 102: 335-341


Schippers JH, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. Curr OpinPlant Biol 29: 121-128


Schmidt R, Schippers JH (2015) ROS-mediated redox signaling during cell differentiation in plants. BBA-Gen Subjects 1850: 1497-1508



http://www.ncbi.nlm.nih.gov/pubmed?term=Mitchell%2DOlds T%2C Schmitt J %282006%29 Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis%2E Nature 441%3A 947%2D952&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441: 947-952

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mitchell-Olds&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Genetic mechanisms and evolutionary significance of natural variation 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=Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Mitchell-Olds&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Murmu J%2C Bush MJ%2C DeLong C%2C Li S%2C Xu M%2C Khan M%2C Malcolmson C%2C Fobert PR%2C Zachgo S%2C Hepworth SR %282010%29 Arabidopsis basic leucine%2Dzipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development%2E Plant Physiol 154%3A 1492%2D1504&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR (2010) Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 154: 1492-1504

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Murmu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther 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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Montrichard F%2C Alkhalfioui F%2C Yano H%2C Vensel WH%2C Hurkman WJ%2C Buchanan BB %282009%29 Thioredoxin targets in plants%3A the first 30 years%2E J Proteomics 72%3A 452%2D474&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72: 452-474

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Montrichard&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Thioredoxin targets in plants: the first 30 years&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Montrichard&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Montano SJ%2C Lu J%2C Gustafsson TN%2C Holmgren A %282014%29 Activity assays of mammalian thioredoxin and thioredoxin reductase%3A fluorescent disulfide substrates%2C mechanisms%2C and use with tissue samples%2E Anal Biochem 449%3A 139%2D146&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Montano SJ, Lu J, Gustafsson TN, Holmgren A (2014) Activity assays of mammalian thioredoxin and thioredoxin reductase: fluorescent disulfide substrates, mechanisms, and use with tissue samples. Anal Biochem 449: 139-146

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Montano&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Motohashi K%2C Koyama F%2C Nakanishi Y%2C Ueoka%2DNakanishi H%2C Hisabori T %282003%29 Chloroplast cyclophilin is a target protein of thioredoxin%2E J Biol Chem 278%3A 31848%2D31852&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T (2003) Chloroplast cyclophilin is a target protein of thioredoxin. J Biol Chem 278: 31848-31852

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http://www.ncbi.nlm.nih.gov/pubmed?term=Motte H%2C Vercauteren A%2C Depuydt S%2C Landschoot S%2C Geelen D%2C Werbrouck S%2C Goormachtig S%2C Vuylsteke M%2C Vereecke D %282014%29 Combining linkage and association mapping identifies RECEPTOR%2DLIKE PROTEIN KINASE1 as an essential Arabidopsis shoot regeneration gene%2E Proc Natl Acad Sci USA 111%3A 8305%2D8310&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Motte H, Vercauteren A, Depuydt S, Landschoot S, Geelen D, Werbrouck S, Goormachtig S, Vuylsteke M, Vereecke D (2014) Combining linkage and association mapping identifies RECEPTOR-LIKE PROTEIN KINASE1 as an essential Arabidopsis shoot regeneration gene. Proc Natl Acad Sci USA 111: 8305-8310

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nelson BK%2C Cai X%2C Nebenf�hr A %282007%29 A multicolored set of in vivo organelle markers for co%2Dlocalization studies in Arabidopsis and other plants%2E Plant J 51%3A 1126%2D1136&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Nelson BK, Cai X, Nebenf�hr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51: 1126-1136

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nelson&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rogers H%2C Munn�%2DBosch S %282016%29 Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence%3A similar but different%2E Plant Physiol 171%3A 1560%2D1568&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rogers H, Munn�-Bosch S (2016) Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: similar but different. Plant Physiol 171: 1560-1568

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rouhier N%2C Cerveau D%2C Couturier J%2C Reichheld JP%2C Rey P %282015%29 Involvement of thiol%2Dbased mechanisms in plant development%2E BBA%2DGen Subjects 1850%3A 1479%2D1496&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rouhier N, Cerveau D, Couturier J, Reichheld JP, Rey P (2015) Involvement of thiol-based mechanisms in plant development. BBA-Gen Subjects 1850: 1479-1496

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http://www.ncbi.nlm.nih.gov/pubmed?term=Sandalio L%2C Romero%2DPuertas M %282015%29 Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks%2E Ann Bot 116%3A 475%2D485&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sandalio L, Romero-Puertas M (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann Bot 116: 475-485

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sandalio&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Schiantarelli E%2C De la Pe�a A%2C Candela M %282001%29 Use of recombinant inbred lines %28RILs%29 to identify%2C locate and map major genes and quantitative trait loci involved with in vitro regeneration ability in Arabidopsis thaliana%2E Theor Appl Genet 102%3A 335%2D341&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schiantarelli E, De la Pe�a A, Candela M (2001) Use of recombinant inbred lines (RILs) to identify, locate and map major genes and quantitative trait loci involved with in vitro regeneration ability in Arabidopsis thaliana. Theor Appl Genet 102: 335-341

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http://www.ncbi.nlm.nih.gov/pubmed?term=Schippers JH%2C Foyer CH%2C van Dongen JT %282016%29 Redox regulation in shoot growth%2C SAM maintenance and flowering%2E Curr Opin Plant Biol 29%3A 121%2D128&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schippers JH, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. Curr Opin Plant Biol 29: 121-128

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http://www.ncbi.nlm.nih.gov/pubmed?term=Schmidt R%2C Schippers JH %282015%29 ROS%2Dmediated redox signaling during cell differentiation in plants%2E BBA%2DGen Subjects 1850%3A 1497%2D1508&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Schmidt R, Schippers JH (2015) ROS-mediated redox signaling during cell differentiation in plants. BBA-Gen Subjects 1850: 1497-1508

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=ROS-mediated redox signaling during cell differentiation 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=ROS-mediated redox signaling during cell differentiation in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schmidt&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Scofield S, Dewitte W, Murray JAH (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development ofreproductive meristematic tissues in Arabidopsis. Plant J 50: 767-781


Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatialregulation are located intragenically. Plant Cell 9: 355-365


Soto D, Cordoba JP, Villarreal F, Bartoli C, Schmitz J, Maurino VG, Braun HP, Pagnussat GC, Zabaleta E (2015) Functionalcharacterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I in Arabidopsis thaliana. Plant J83: 831-844


Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsisenzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17: 616-627


Su YH, Zhao XY, Liu YB, Zhang CL, O'Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stemcell renewal during somatic embryogenesis in Arabidopsis. Plant J 59: 448-460


Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway.Dev Cell 18: 463-471


Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformationalcharges of NPR1 via S-nitrosylation and thioredoxins. Science 321: 952-956


Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2014) Differential geneand transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoco 7: 562-578


Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation todifferentiation in the root. Cell 143: 606-616


van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10: 2009-2010Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Velázquez I, Valencia S, López-Lera A, de la Peña A, Candela M (2004) Analysis of natural allelic variation in in vitro organogenesisof Arabidopsis thaliana. Euphytica 137: 73-79


Viola IL, Güttlein LN, Gonzalez DH (2013) Redox modulation of plant developmental regulators from the class I TCP transcriptionfactor family. Plant Physiol 162: 1434-1447


Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance inmaize seedlings. Nat Genet 48: 1233-1241

Pubmed: Author and Title www.plantphysiol.orgon July 21, 2017 - Published by Downloaded from


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http://search.crossref.org/?page=1&rows=2&q=Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616

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http://search.crossref.org/?page=1&rows=2&q=van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10: 2009-2010

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http://search.crossref.org/?page=1&rows=2&q=Viola IL, G�ttlein LN, Gonzalez DH (2013) Redox modulation of plant developmental regulators from the class I TCP transcription factor family. Plant Physiol 162: 1434-1447

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http://www.ncbi.nlm.nih.gov/pubmed?term=Wang X%2C Wang H%2C Liu S%2C Ferjani A%2C Li J%2C Yan J%2C Yang X%2C Qin F %282016%29 Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings%2E Nat Genet 48%3A 1233%2D1241&dopt=abstract


CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops - production, perception, regulation. Curr Opin Plant Biol 16:575-582


Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetalprogrammed cell death and pollen development in Arabidopsis. Plant Cell 26: 2007-2023


Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006) A molecular framework for plant regeneration. Science 311: 385-388


Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria.Plant Cell Physiol 54: 875-892


Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts. JBiol Chem 290: 14278-14288


Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-Loop NTPase regulates quiescent center cell division and distal stemcell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12: e1006175


Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F (2015) Oxidative post-translational modifications ofcysteine residues in plant signal transduction. J Exp Bot 66: 2923-2934


Zhang TQ, Lian H, Zhou CM, Xu L, Jiao Y, Wang JW (2017) A Two-Step Model for de novo Activation of WUSCHEL during PlantShoot Regeneration. The Plant Cell 29: 1073-1087


Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Bio 61: 49-64Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis CALCIUM-DEPENDENT PROTEINKINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells underdrought stress. Plant Cell 27: 1445-1460



http://search.crossref.org/?page=1&rows=2&q=Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48: 1233-1241

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Wang&hl=en&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Wrzaczek M, Brosch� M, Kangasj�rvi J (2013) ROS signaling loops - production, perception, regulation. Curr Opin Plant Biol 16: 575-582

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http://search.crossref.org/?page=1&rows=2&q=Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26: 2007-2023

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http://search.crossref.org/?page=1&rows=2&q=Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006) A molecular framework for plant regeneration. Science 311: 385-388

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=A molecular framework for plant regeneration&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 molecular framework for plant regeneration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Noguchi K%2C Motohashi K%2C Hisabori T %282013%29 Systematic exploration of thioredoxin target proteins in plant mitochondria%2E Plant Cell Physiol 54%3A 875%2D892&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54: 875-892

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yoshida&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Systematic exploration of thioredoxin target proteins in plant mitochondria&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=Systematic exploration of thioredoxin target proteins in plant mitochondria&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshida&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Hara S%2C Hisabori T %282015%29 Thioredoxin selectivity for thiol%2Dbased redox regulation of target proteins in chloroplasts%2E J Biol Chem 290%3A 14278%2D14288&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts. J Biol Chem 290: 14278-14288

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yoshida&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts&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=Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshida&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yu Q%2C Tian H%2C Yue K%2C Liu J%2C Zhang B%2C Li X%2C Ding Z %282016%29 A P%2DLoop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root%2E PLoS Genet 12%3A e1006175&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12: e1006175

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yu&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root.&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 P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Waszczak C%2C Akter S%2C Jacques S%2C Huang J%2C Messens J%2C Van Breusegem F %282015%29 Oxidative post%2Dtranslational modifications of cysteine residues in plant signal transduction%2E J Exp Bot 66%3A 2923%2D2934&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F (2015) Oxidative post-translational modifications of cysteine residues in plant signal transduction. J Exp Bot 66: 2923-2934

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Waszczak&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Oxidative post-translational modifications of cysteine residues in plant signal transduction&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=Oxidative post-translational modifications of cysteine residues in plant signal transduction&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Waszczak&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang TQ%2C Lian H%2C Zhou CM%2C Xu L%2C Jiao Y%2C Wang JW %282017%29 A Two%2DStep Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration%2E The Plant Cell 29%3A 1073%2D1087&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang TQ, Lian H, Zhou CM, Xu L, Jiao Y, Wang JW (2017) A Two-Step Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration. The Plant Cell 29: 1073-1087

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A Two-Step Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration&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 Two-Step Model for de novo Activation of WUSCHEL during Plant Shoot Regeneration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao Y %282010%29 Auxin biosynthesis and its role in plant development%2E Annu Rev Plant Bio 61%3A 49%2D64&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Bio 61: 49-64

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhao&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Auxin biosynthesis and its role in plant 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=Auxin biosynthesis and its role in plant development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhao&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zou JJ%2C Li XD%2C Ratnasekera D%2C Wang C%2C Liu WX%2C Song LF%2C Zhang WZ%2C Wu WH %282015%29 Arabidopsis CALCIUM%2DDEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid%2Dmediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress%2E Plant Cell 27%3A 1445%2D1460&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zou JJ, Li XD, Ratnasekera D, Wang C, Liu WX, Song LF, Zhang WZ, Wu WH (2015) Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27: 1445-1460

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zou&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought 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=Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zou&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1


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Thioredoxin-Mediated ROS Homeostasis Explains …...The work was supported by the National Natural Science Foundation of China (31270231, 10 91217308). 11 12 2 These authors contributed