Extensive Post-Transcriptional Regulation of Nuclear Gene ... · 5/28/2019 · 7 Title: Extensive Post-Transcriptional Regulation of Nuclear Gene Expression 8 by Plastid Retrograde

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Short title: Gene regulation in retrograde signaling 1

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The author responsible for distribution of materials integral to the findings presented in this 3

article in accordance with the policy described in the Instructions for Authors 4

(www.plantphysiol.org) is: Ralph Bock ([email protected]). 5

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Title: Extensive Post-Transcriptional Regulation of Nuclear Gene Expression 7

by Plastid Retrograde Signals 8

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Author names and affiliations: 10

Guo-Zhang Wu1*, Etienne H. Meyer1, 2, Si Wu1, 3 and Ralph Bock1* 11

12 1Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, D-14476 13

Potsdam-Golm, Germany 14 2Present address: Martin-Luther-University Halle-Wittenberg, Institute of Plant Physiology, 15

Weinbergweg 10, 06120 Halle, Germany 16 3Present address: Department of Genetics, School of Medicine, Stanford University, Stanford, 17

CA 94305, USA 18

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Number of figures: 7 20

Number of tables: 1 21

Number of supplemental items: 14 22

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One sentence summary: Translational and post-translational regulation play a crucial role in the 24

plastid gene expression pathway of retrograde signaling and supports a function of GUN1 in 25

plastid proteostasis. 26

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Author contributions 28

Plant Physiology Preview. Published on May 28, 2019, as DOI:10.1104/pp.19.00421

Copyright 2019 by the American Society of Plant Biologists

https://plantphysiol.orgDownloaded on November 24, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://plantphysiol.org

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G.-Z.W. and R.B. conceived and designed the research. G.-Z.W. performed most of the 29

experiments. E.H.M. conducted the mass spectrometry for proteomic analyses. S.W. statistically 30

analyzed the microarray data. G.-Z.W. and R.B. integrated the data and wrote the manuscript. 31

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Funding: This research was financed by the Max Planck Society and a grant from the Deutsche 33

Forschungsgemeinschaft to R.B. (SFB TR175). 34

35 *For correspondence: [email protected] (R.B.) or [email protected] (G.-Z. 36

Wu) 37

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ABSTRACT 40

41

Retrograde signals emanate from the DNA-containing cell organelles (plastids and mitochondria) 42

and control the expression of a large number of nuclear genes in response to environmental 43

and developmental cues. Previous studies on retrograde signaling have mainly analyzed the 44

regulation of nuclear gene expression at the transcript level. To determine the contribution of 45

translational and post-translational regulation to plastid retrograde signaling, we combined label-46

free proteomics with transcriptomic analysis of Arabidopsis (Arabidopsis thaliana) seedlings and 47

studied their response to interference with the plastid gene expression (PGE) pathway of 48

retrograde signaling. By comparing the proteomes of the genomes uncoupled 1 (gun1) and gun5 49

mutants with wild-type , we show that GUN1 is critical in the maintenance of plastid protein 50

homeostasis (proteostasis) when plastid translation is blocked. Combining transcriptomic and 51

proteomic analyses of wild-type and gun1, we identified 181 highly translationally or post-52

translationally regulated (HiToP) genes. We demonstrate that HiToP photosynthesis-associated 53

nuclear genes (PhANGs) are largely regulated by translational repression, while HiToP 54

ribosomal protein genes are regulated post-translationally – likely at the level of protein stability 55

without the involvement of GUN1. Our findings suggest distinct post-transcriptional control 56

mechanisms of nuclear gene expression in response to plastid-derived retrograde signals. They 57

also reveal a role for GUN1 in the translational regulation of several PhANGs, and highlight 58

extensive post-translational regulation that does not necessitate GUN1. This study advances our 59

understanding of the molecular mechanisms underlying intracellular communication, and 60

provides new insight into cellular responses to impaired plastid protein biosynthesis. 61

62

Keywords: chloroplast, retrograde signaling, translational repression, protein stability, 63

proteostasis 64

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4

INTRODUCTION 67

Intracellular communication between different cell compartments is essential to optimize gene 68

expression for differentiation, development and responses to environmental challenges (Parikh et 69

al., 1987; Cottage et al., 2010; Estavillo et al., 2011; Xiao et al., 2012; Esteves et al., 2014). Most 70

protein complexes of plastids and mitochondria are mosaics of organelle-encoded and nucleus-71

encoded subunits. Consequently, tight coordination of gene expression from both genomes is 72

crucial to cellular homeostasis and fitness of the whole organism (Liu and Butow, 2006; Jarvis 73

and Lopez-Juez, 2013; Chan et al., 2016). Already nearly four decades ago, it was realized that 74

defects in plastid protein synthesis can repress the accumulation of nucleus-encoded plastid 75

proteins (Bradbeer et al., 1979). It was proposed that signals emanating from plastids and relayed 76

to the nucleus (later dubbed retrograde signals) control the expression of a large number of 77

nuclear genes and, in this way, help to harmonize the functional state of the plastids with that of 78

the nucleus (Woodson and Chory, 2008; Chan et al., 2016). Over the past decades, substantial 79

progress has been made with identifying signaling components and distinct pathways of 80

retrograde signaling that regulate chloroplast biogenesis (biogenetic control) or control plastids 81

homeostasis in response to environmental stimuli (operational control; Susek et al., 1993; 82

Wagner et al., 2004; Koussevitzky et al., 2007; Pogson et al., 2008; Estavillo et al., 2011; 83

Woodson et al., 2011; Ramel et al., 2012; Xiao et al., 2012). Various potential signaling 84

molecules have been identified, including intermediates of tetrapyrrole biosynthesis (TPB; 85

Strand et al., 2003; Woodson et al., 2011), carotenoid oxidation products (Ramel et al., 2012; 86

Shumbe et al., 2014), isoprenoid precursors (Xiao et al., 2012), phosphoadenosines (Estavillo et 87

al., 2011), hydrogen peroxide (Balazadeh et al., 2012; Maruta et al., 2012) and carbohydrate 88

metabolites (Heinrichs et al., 2012; Vogel et al., 2014). 89

The chloroplast translation inhibitor lincomycin (Lin; Mulo et al., 2003) and the 90

carotenoid biosynthesis inhibitor norflurazon (NF; Oelmuller, 1989) have been widely used to 91

inhibit chloroplast biogenesis and demonstrate the biogenic control exerted by plastid retrograde 92

signaling. Six GENOMES UNCOUPLED (GUN) loci, whose inactivation uncouples nuclear 93

gene expression from proper chloroplast function, have been identified through genetic screens 94

(Susek et al., 1993; Woodson et al., 2011). Five of the six GUN genes (GUN2-6) encode 95

enzymes or regulators of the TPB pathway, underscoring the essential role of TPB-derived 96

retrograde signals in chloroplast biogenesis (Mochizuki et al., 2001; Larkin et al., 2003; von 97



5

Gromoff et al., 2008; Woodson et al., 2011). Inhibition of plastid gene expression (PGE) 98

represses the expression of a number of photosynthesis-associated nuclear genes (PhANGs). 99

Distinct from the other GUN genes, GUN1 is the only known GUN gene that, when defective, 100

results in de-repression of the expression of PhANGs in the presence of both Lin (which inhibits 101

PGE by blocking chloroplast translation) and NF (which affects TPB signaling; Koussevitzky et 102

al., 2007; Wu et al., 2018; Wu et al., 2019). Interestingly, the GUN1 mutation was shown to 103

restore PhANG expression in plastid sigma factor mutants (Woodson et al., 2013), the prors1 104

mutant (defective in prolyl-tRNA synthetase in both chloroplasts and mitochondria; Tadini et al., 105

2016) and the prin2 mutant (affecting a locus required for full expression of genes transcribed by 106

the plastid-encoded RNA polymerase; Kindgren et al., 2012; Díaz et al., 2018). Together, these 107

findings indicate a central role of GUN1 in the PGE pathway of retrograde signaling. 108

The vast majority of studies on retrograde signaling demonstrated regulation of nuclear 109

genes by organellar signals at the transcript level (i.e., mRNA abundance and alternative splicing; 110

Petrillo et al., 2014). Ferredoxin I (Fed-1) transcript abundance was shown to be modulated, in a 111

light-dependent manner, post-transcriptionally at the level of mRNA stability (Elliott et al., 1989; 112

Petracek et al., 1997; Petracek et al., 1998). Loading of Fed-1 mRNA with ribosomes in the light 113

likely results in protection from nucleolytic degradation (Dickey et al., 1994; Dickey et al., 1998). 114

This observation indicates a potential link between retrograde regulation of nuclear gene 115

expression and cytosolic translation. The possible role of translational and post-translational 116

regulation in retrograde signaling is only beginning to draw more attention. For example, the 117

translational response of Arabidopsis (Arabidopsis thaliana) to a shift from low light to high 118

light (which induces operational control of retrograde signaling; Oelze et al., 2014) has been 119

studied, the relationship between accumulation of light-harvesting complex (LHC) proteins and 120

their transcripts upon impaired plastid translation has been analyzed (Krupinska et al., 2019), and 121

an important role of post-translational modifications in mitochondrial retrograde regulation is 122

emerging (Hartl and Finkemeier, 2012). The GOLDEN2-LIKE (GLK) transcriptional activator 123

positively regulates the expression of a large number of PhANGs in plants (Yasumura et al., 124

2005; Waters et al., 2009). It was demonstrated that the expression of GLK1 is controlled by 125

GUN1-dependent retrograde signals (Kakizaki et al., 2009). GLK1 protein accumulation under 126

Lin and NF treatments is regulated post-translationally by protein degradation through the 127

cytosolic ubiquitin proteasome system (UPS; Tokumaru et al., 2017), indicating a role of post-128



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translational regulation in plastid retrograde signaling. GUN1 was also shown to regulate the 129

accumulation of plastid ribosomal protein PRPS1 independent of PRPS1 mRNA abundance, 130

although the underlying mechanism remains to be investigated (Tadini et al., 2016). Overall, the 131

contribution of translational and post-translational regulation to retrograde signaling and to 132

retrograde regulation upon defective transcriptional regulation (e.g., in gun mutants), is still 133

largely unknown. 134

To systematically investigate the contribution of translational and post-translational 135

mechanisms to plastid retrograde regulation, we investigated the translational and post-136

translational regulation emanating from the PGE pathway in the wild type and the gun1 mutant. 137

Our results demonstrated that, although PhANG expression is de-repressed in gun1 at the 138

transcript level, inhibition of plastid translation triggers similar changes in the proteomes of gun1 139

and the wild type, indicating strong translational and post-translational components in retrograde 140

responses in the PGE pathway. We identified 181 highly translationally or post-translationally 141

regulated (HiToP) genes in the wild type and classified them into two classes that differ in their 142

patterns of gene regulation. We further show that HiToP PhANGs are largely regulated by 143

translational repression, while HiToP ribosomal protein-encoding genes are regulated post-144

translationally, likely through protein degradation. Our results suggest that the translational 145

repression of PhANGs is dependent on GUN1, while the post-translational regulation of 146

ribosomal protein-encoding genes does not require the function of GUN1. 147

148

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7

RESULTS 150

GUN1 Regulates Plastid Proteostasis upon Interference with Retrograde Signaling 151

In order to understand the regulation of nuclear genes by chloroplast retrograde signals at the 152

protein level, we performed proteomic analyses of the wild type and the gun1 mutant. To this 153

end, plants were grown under control conditions or treated with Lin to interfere with the PGE 154

pathway of retrograde signaling (Figure 1; Supplemental Dataset S1). Since the PGE pathway is 155

mainly active during the first few days after germination when massive chloroplast biogenesis is 156

occurring (Oelmuller et al., 1986), we germinated and grew the seedlings in the dark for 5 days 157

followed by 2 days in continuous light to mimic the chloroplast biogenesis events occurring 158

during the first days after germination. Also, using this experimental setup, enough material for 159

proteomic analyses could be obtained. We included the gun5 mutant as a control, since GUN5 160

only de-represses PhANG expression under NF treatment, but not under Lin treatment 161

(Mochizuki et al., 2001; Hernandez-Verdeja and Strand, 2018). 162

Plastid-encoded proteins account for ~18% of the total cellular protein under control 163

conditions. The large subunit of the ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco; 164

RbcL) accounts for approximately half of this amount (Supplemental Figure S1A). Upon Lin 165

treatment, plastid-encoded proteins account for only ~0.17% of the total cellular protein. By 166

contrast, mitochondrially encoded proteins show no significant change in their abundance 167

(Supplemental Figure S1B), confirming the specific inhibition of plastid translation by Lin 168

(Mulo et al., 2003). 169

While the gun1 mutant does not show a visible phenotype under normal growth conditions, 170

the gun5 mutant displays a pale green phenotype (Mochizuki et al., 2001; Koussevitzky et al., 171

2007). Consistent with the absence of a visual mutant phenotype, the proteome of gun1 does not 172

show many differences to the wild type under control conditions. We only identified 28 proteins 173

that are differentially expressed between the wild type and gun1 (Supplemental Table S1). This 174

set of proteins did not show any particular enrichment in functional classification or cellular 175

compartment (Figure 1A; Supplemental Table S1). By contrast, the proteome of gun5 shows 176

large differences compared to that of the wild type. The number of proteinsfound to be 177

differentially expressed in gun5 compared to the wild type was 366 (Figure 1B; Supplemental 178

Dataset S1). Among these, 262 proteins are down-regulated and 104 proteins are up-regulated in 179

gun5. In agreement with the pale green phenotype, 172 of the 262 down-regulated proteins are 180



8 localized in the chloroplast (according to SUBA4; http://suba.live/), including subunits of 181



9

different photosynthetic complexes and proteins involved in chloroplast biogenesis. By contrast, 182

only 4 chloroplast-localized proteins were identified among the 104 up-regulated proteins 183

(Figure 1B; Supplemental Dataset S1): ADP-glucose pyrophosphorylase (APL2; catalyzes the 184

first and rate limiting step in starch biosynthesis), aldehyde reductase (ChlADR), glutamine 185

phosphoribosylpyrophosphate amidotransferase 1 (ASE1; a key enzyme in the pathway of purine 186

nucleotide biosynthesis) and ferretin 1 (FER1; ferric iron binding). 187

When the seedlings were grown in the presence of Lin to affect the PGE pathway of 188

retrograde signaling, the differences between the wild type and gun5 became smaller, with only 189

98 proteins showing differential expression ( Figure 1A,B). Moreover, the plastid-localized 190

proteins (21 out of 98) were no longer as strongly overrepresented as in the control conditions. 191

This can potentially be explained by the plastids of the wild type and gun5 both remaining 192

undifferentiated upon Lin treatment. In contrast to the increased similarity between the 193

proteomes of the wild type and gun5, the proteome of gun1 shows strongly increased differences 194

to that of the wild type (Figure 1A). Compared to the control conditions, now 217 proteins are 195

identified as differentially expressed between the wild type and gun1 (Figure 1B; Supplemental 196

Dataset S1). Among these, 145 proteins are down-regulated and 72 up-regulated. Interestingly, 197

more than 88% (128 out of 145) of the down-regulated proteins are plastid-localized (Figure 1B). 198

By contrast, only ~19% of the proteins up-regulated in gun1 are localized in the plastids, and 199

only ~29% (15 out of 51) of the proteins down-regulated in gun5 are plastid-localized. The large-200

scale down-regulation of plastid proteins in gun1 upon Lin treatment indicates an important role 201

of GUN1 in the maintenance of plastid protein homeostasis (proteostasis) when the PGE 202

pathway of retrograde signaling is altered (Lin treatment). We further investigated the 128 down-203

regulated plastid proteins. Interestingly, when compared within the same genotype in the 204

presence versus absence of Lin, only half (64 out of 128) of these proteins show more than two-205

fold repression by Lin in the wild type (Supplemental Dataset S2). This indicates that (i) proteins 206

that are repressed by Lin in the wild type are even more strongly repressed in gun1, and (ii) 207

proteins that are unchanged or even up-regulated in the wild type, are down-regulated in gun1. 208

Many of the 128 proteins are directly or indirectly involved in proteostasis, including a large 209

number of ribosomal proteins (14), proteases (9), rRNA processing factors (8) and proteins 210

involved in redox regulation (8; Figure 1C; Supplemental Data S2). This observation provides 211

further evidence for plastid proteostasis in gun1 differing substantially from that in the wild type 212



10

upon Lin treatment. The proteomes of gun1 and the wild type do not show many differences 213

under control conditions, suggesting that GUN1 exerts its role in the regulation of plastid 214

proteostasis only (or predominantly) under conditions when retrograde signaling is altered. 215

216

Strong Translational and Post-Translational Regulation Occurs when Retrograde 217

Signaling Is Affected 218

The defective repression of PhANGs in gun1 upon Lin treatment is expected to result in higher 219

PhANG protein accumulation compared to the wild type. However, our proteomic analyses of 220

the wild type and the gun1 mutant revealed that this is not the case (Figure 1; Supplemental 221

Dataset S1). We identified only 14 plastid-localized proteins that over-accumulate in gun1 222

relative to the wild type (Supplemental Table S2). Ten out of these 14 proteins are typical 223

PhANGs, including three subunits of LHC, two subunits of photosystem II (PSII), one subunit 224

each of PSI and the NAD(P)H dehydrogenase (NDH) complex, carbonic anhydrases (CA1 and 225

CA2) and fructose-bisphosphate aldolase 5 (FBA5). 226

To resolve this seeming contradiction, we analyzed gene expression at the RNA level by 227

whole-genome microarrays to enable side-by-side analysis of gene regulation at the transcript 228

accumulation versus protein accumulation levels. From the proteomic datasets, all proteins that 229

were detected in at least two biological replicates of at least one condition (genotype or 230

treatment) were selected for further analysis. Since oligo(dT) primer was used for first-strand 231

cDNA synthesis for the microarray experiments (and organellar transcripts are not normally 232

polyadenylated), we excluded genes encoded in the plastid and mitochondrial genomes. 233

Applying these criteria, 5449 genes with transcript and protein expression data could be used for 234

transcript-protein co-analysis (Figure 2; Supplemental Dataset S3). When we compared 235

transcript accumulation in the wild type and the gun1 mutant in the control conditions with that 236

upon Lin treatment, the correlation of expression changes in the wild type and gun1 was found to 237

be very low (Pearson correlation coefficient: 0.30; Figure 2A). We identified only 26 genes that 238

show differential expression at the transcript level between the wild type and gun1 under control 239

conditions (Supplemental Table S3). Interestingly, the cytosolic chaperones involved in protein 240

quality control (PQC), including two small heat shock proteins (HSP17.6A and HSP17.6II), 241

HSP90.1, HSP70-2 and HSP70-4, and the transcription factor HSFA2 (involved in the responses 242

to heat stress and accumulation of misfolded proteins in the cytosol), were up-regulated in gun1. 243



11

The low correlation in response to Lin treatment indicates a different response of gun1 compared 244

to the wild type. The differences are not just caused by the de-repression of PhANGs in gun1, 245

since a large number of non-PhANGs is differentially expressed between the two genotypes 246

upon Lin treatment (Supplemental Dataset S4). Interestingly, when we compared the changes at 247

the protein level, the wild type and the gun1 mutant responded surprisingly similar to the Lin 248

treatment (Pearson correlation coefficient: 0.81; Figure 2B). This indicates that, although the 249

response of gun1 at the transcript level is very different from that of the wild type, strong 250

translational and post-translational regulation overrides many of the changes in transcripts 251

abundance, thus making the response at the protein level more similar. In agreement with this, 252

although 773 genes show differential expression (FDR<0.05, fold change>2) at the transcript 253

level between the wild type and gun1 under Lin treatment (of which 254 can be detected by mass 254



12

spectrometry at the protein level), only 56 proteins show more than two-fold changes in the same 255

direction as their transcripts (i.e., both go up or down; Supplemental Dataset S4). 256

257

Type I and Type II Highly Translationally or Post-translationally Regulated (HiToP) 258

Genes 259

To further understand how gene expression is regulated by retrograde signaling, we performed a 260

correlation analysis of transcripts and proteins in control conditions compared to Lin treatment 261

for each genotype (Figure 3A,B). In the wild type, some PhANGs, such as LHCB1.4 and CA1, 262

show a good correlation between mRNA and protein, in that both are repressed in the presence 263

of Lin. For other PhANGs, for example, the small subunit of Rubisco (RBCS1B and RBCS3B), 264

subunits of PSI (PsaG, PsaL and PsaD), and the calcium sensing receptor (CaSR), the down-265

regulation at the protein level is much stronger than that at the transcripts level (Figure 3A; 266

Supplemental Dataset S3). This observation suggests that, also in the wild type, strong 267

translational and/or post-translational regulation is exerted in response to altered PGE pathway of 268

retrograde signaling (Lin treatment). However, compared to the wild type, the regulation is much 269

stronger in gun1 (Figure 3B). For example, the transcripts of all genes mentioned above did not 270

show a substantial repression by Lin treatment, but all proteins, except CA1, were strongly 271

down-regulated (Figure 3B; Supplemental Dataset S3). By contrast, the expression of the non-272

PhANG lipoxygenase 2 (LOX2) gene is repressed at the mRNA and protein levels both in the 273

wild type and gun1 (Figure 2A,B; Supplemental Figure S2). 274

Our observation that there is strong translational and post-translational regulation also in 275

the wild type suggests that this type of regulation is a general control mechanism in response to 276

Lin treatment (altering the PGE pathway). To explore the extent of translational and post-277

translational regulation more systematically, we analyzed transcript and protein accumulation in 278

the wild type to identify highly translationally or post-translationally regulated (HiToP) genes. 279

We classified HiToP genes into two types: type I comprising genes whose expression changes at 280

the protein level more than 8-fold, but less than twofold at the transcript level (log2 protein 281

control/Lin >3 or <-3, but -1< log2 transcript control/Lin <1), and type II comprising genes that, 282

although their expression changes at the transcript level more than twofold, the super-ratio of 283

protein change to transcript change (reflecting the correlation of the transcript with its protein 284

product, with a large super-ratio indicating low correlation and thus, strong translational or post-285



13 translational regulation) was higher than 8 (log2 transcript control/Lin >1 or < -1, but log2 super-286



14

ratio >3 or <-3). By these criteria, we identified 181 HiToP genes in the wild type, with 130 of 287

them being down-regulated and 51 being up-regulated upon Lin treatment (Figure 3A,C; 288

Supplemental Dataset S5). Among the 181 HiToP genes, 127 genes were identified as type I, and 289

54 as type II genes. Importantly, most of the down-regulated HiToP genes (108 out of 130) 290

encode plastid-localized proteins, thus underscoring the specific action of Lin treatment on 291

plastid retrograde signaling. 292

We then further analyzed the functional annotation of the 108 down-regulated HiToP 293

genes whose protein products localize to plastids, to determine if they are enriched in specific 294

pathways or macromolecular complexes (Figure 3D; Supplemental Dataset S5). Interestingly, 295

genes for PSI and PSII subunits were mainly among the type II HiToP genes, indicating that they 296

are down-regulated also at the transcripts level. By contrast, most of the genes for ribosomal 297

subunits and genes involved in proteostasis were identified as type I. Of the 24 type I HiToP 298

genes with a more than 16-fold down-regulation at the protein level (log2 protein control/Lin >4), 299

7 encode ribosomal proteins (Table 1). 300

For comparison, we also analyzed HiToP genes in gun1, where we identified 326 HiToP 301

genes in total (Figure 3B,C; Supplemental Dataset S5). While the numbers of up-regulated genes 302

and down-regulated genes that encode non-plastid-localized proteins in gun1 are similar to those 303

in the wild type, the number of down-regulated chloroplast-localized proteins is substantially 304

larger in the gun1 mutant (Figure 3C). Interestingly, among the 326 HiToP genes in gun1, only 305

21 genes were identified as type II genes (Figure 3B; Supplemental Dataset S5). By contrast, 306

more than 93% (305 out of 326) HiToP genes in gun1 were identified as type I genes (less than 307

two-fold change at the transcript level), further indicating that most of the genes are regulated 308

post-transcriptionally. 309

To further analyze the regulation in gun1, we focused on the type I genes that are down-310

regulated at the protein level (Figure 3A,B, green box). We identified 85 and 261 down-311

regulated type I genes in the wild type and gun1, respectively (Figure 3E). 66 genes overlap 312

between the two sets. Of the 195 genes only identified in gun1, 182 encode plastid-localized 313

proteins (Figure 3E). Gene ontology (GO) analysis shows that they are enriched in functions 314

related to PSI, PSII and plastoglobules (Figure 3F). These results indicate that the expression of 315

many PhANGs is repressed in gun1 at the level of protein accumulation by translational or post-316

translational mechanisms. 317



15

To confirm the pattern of post-transcriptional regulation seen in our microarray and mass 318

spectrometry studies, we selected several genes for northern blot and western blot analyses 319

(Figure 4). Based on antibody availability, we chose LHCA4, LHCB1 and RBCS as PhANGs, and 320

RPL4 as an example of a plastid ribosomal protein. While the degree of repression of transcript 321

accumulation varied between the four genes (with LHCB1 mRNA accumulation being most 322

strongly down-regulated; Figure 4A), the proteins were all below the detection limit of the 323

immunoblot (Figure 4B). This finding lends further support to the idea that, as gun1 is unable to 324

inhibit nuclear gene expression at the transcript level, the repression of plastid-localized proteins 325

in gun1 relies largely on down-regulation at the translational and/or post-translational levels, to 326

ultimately reach a similarly low protein level as in the wild type. 327

328

Repression of LHCB Accumulation in gun1 by Translational Inhibition 329

To distinguish between translational and post-translational regulation, polysome profiles were 330

analyzed for several mRNAs. We first examined genes whose transcripts are largely repressed in 331

the wild type, but not in gun1, to determine how failure of accumulation of the corresponding 332

proteins continues to occur in spite of the loss of GUN1. In comparison to LHCA4 and RBCS, 333

mRNA accumulation of LHCB1 was very strongly repressed by Lin treatment in the wild type, 334

but not in gun1 (Figure 4A; Supplemental Figure S3). LHCB transcripts were also found to be 335

dramatically repressed in de-etiolating pea seedlings in the presence of NF compared to the mild 336

repression of RBCS and Fed-1 transcripts (Sagar et al., 1988). When we analyzed the polysome 337

profiles of LHCB1 in both genotypes (Figure 5), the transcripts in the wild type were found to be 338

repressed to nearly undetectable levels, consistent with the microarray data. By contrast, LHCB1 339

continues to be expressed in gun1 in the presence of Lin (Figs. 4A and 5). Remarkably, while a 340

large proportion of the mRNA is present in the polysome-containing fractions 9-11 under control 341

conditions, polysome association is repressed by Lin treatment (Figure 5). The redistribution of 342

LHCB1 transcripts from polysome fractions in control conditions to the free mRNA pool upon 343

Lin treatment suggests translational repression of LHCB1 in gun1 in response to Lin treatment. 344

345

PhANGs and Ribosomal Proteins Are Regulated by Translational and Post-Translational 346

Repression, Respectively, in Response to Chloroplast Translation Inhibition 347



16

We have identified 108 chloroplast-localized HiToP genes that are down-regulated in response to 348

Lin treatment in the wild type (Figure 3C). To shed light on the underlying mechanisms of post-349

transcriptional regulation, we analyzed polysome profiles for a set of PhANGs (mainly identified 350

as type II HiToP genes) and non-PhANGs (e.g., nuclear genes encoding plastid ribosome 351



17

proteins which mainly had been identified as type I HiToP genes; Figure 3D). As examples of 352

PhANGs, we analyzed RBCS and LHCA4, two classical genes regulated by retrograde signals 353

(Woodson et al., 2011; Kindgren et al., 2012; Woodson et al., 2013). Different from LHCB1 354

genes, the transcripts of LHCA4 and RBCS still accumulate under Lin treatment (Figure 4A), but 355



18

the proteins are below the detection limit of immunoblots (Figure 4B). As examples of 356

chloroplast ribosomal proteins, we chose PSRP5 and RPL4 (Supplemental Dataset S5), because 357

(i) PSRP5 was ranked as the strongest post-transcriptionally regulated ribosomal protein gene 358



19

(Table 1), and (ii) an antibody against RPL4 is available, thus allowing us to examine protein 359

accumulation by immunoblotting (Figure 4B). 360

Analysis of polysome profiles of RBCS and LHCA4 mRNAs demonstrated that translation 361

of both transcripts was strongly repressed, as revealed by strong reduction of mRNA abundance 362

in polysome-containing fractions (fractions 8-10 for RBCS and 9-11 for LHCA4, respectively; 363

Figure 6A; Supplemental Figure S4A). This observation suggests that expression of these HiToP 364

PhANGs is largely controlled by translational repression. 365

Interestingly, the ribosomal protein-coding genes we tested show the opposite behavior. 366

Unlike the RBCS and LHCA4, both PSRP5 and RPL4 show increased translation in response to 367

Lin treatment (Figure 6B; Supplemental Figure S4B). The PSRP5 mRNA accumulated in 368

polysome fractions 7-9 in the untreated control, but shifted to fractions 9-11 under Lin treatment, 369

indicating denser loading with ribosomes. Similarly, the RPL4 mRNA was mainly present in 370

polysome fraction 10 and shifted to fraction 12 in response to Lin treatment. Considering the 371

undetectably low accumulation of these ribosomal proteins under Lin treatment (Figure 4B), the 372

repression of their expression obviously occurs at the post-translational level, likely by 373

regulation of protein stability/degradation. 374

375

GUN1-Dependent Plastid Retrograde Signals from the PGE Pathway Regulate Cytosolic 376

Translation 377

To examine if the translational regulation discovered in this study is regulated by GUN1-378

dependent retrograde signals, we analyzed the polysome profiles of PhANGs and ribosomal 379

protein-coding genes in the gun1 mutant (Figure 7 and Supplemental Figure S5). Interestingly, 380

the translational repression of RBCS and LHCA4 and, to a lesser extent, the translational up-381

regulation of ribosomal protein-coding genes (PSRP5 and RPL4) observed in the wild type is 382

compromised in gun1. These findings suggest that the cytosolic translational re-adjustment in 383

response to altered PGE-derived retrograde signals requires the function of GUN1. In order to 384

overcome the defective transcriptional and translational regulation (e.g., of RBCS and LHCA4), 385

post-translational control mechanisms set in when GUN1 is absent. Therefore, this post-386

translational control is likely independent of GUN1. 387

388

389



20

DISCUSSION 390

391



21

Signals emanating from organelles have been shown to coordinate nuclear gene expression with 392

organelle function (Jia et al., 1997; Butow and Avadhani, 2004; Chi et al., 2013; Hernandez-393

Verdeja and Strand, 2018). Previous studies that established the concept of retrograde regulation 394

largely focused on transcriptional control and transcript accumulation (Mochizuki et al., 2001; 395

Strand et al., 2003; Koussevitzky et al., 2007; Lee et al., 2007; Estavillo et al., 2011; Xiao et al., 396



22

2012). To explore the possible role and the extent of translational and post-translational 397

regulation, we here analyzed gene expression in the PGE pathway of plastid retrograde signaling 398

by comparing transcriptomes and proteomes of wild-type plants with those of knock-out mutants 399

for the proposed central regulator of retrograde signaling GUN1 upon Lin treatment 400

(Koussevitzky et al., 2007; Wu et al., 2019). 401

Interestingly, although the transcriptomes of the wild type and gun1 in response to Lin 402

treatment differ very strongly, the proteomes of the two genotypes are much closer to each other 403

(Figure 2). GO analysis performed with the 182 down-regulated type I HiToP genes whose 404

protein products localize to plastids shows that the GO terms for photosynthesis-related functions 405

were significantly overrepresented (Figure 3F). Many of the PhANG-encoded proteins 406

accumulate to undetectably low levels in both the wild type and gun1 (Figure 4B). The 407

repression of PhANG expression in gun1 predominantly does not occur at the translational level 408

(only repression of LHCB translation was observed). In fact, the translation inhibition of LHCA4 409

and RBCS genes in gun1 is even weaker than in the wild type (Figure 6 and Figure 7). Our 410

results suggest that the post-transcriptional repression of PhANG expression in gun1 happens 411

largely post-translationally, at the level of protein degradation. 412

When we compared the transcriptomes and proteomes of the wild type, it became evident 413

that translational and post-translational regulation is crucial also in wild-type plants. We have 414

identified 181 HiToP genes in the wild type. By comparing the polysome profiles of the different 415

types of HiToP genes, we observed that the translation of two classes of HiToP PhANGs tested 416

(RBCS genes and LHCA4) was strongly repressed. This observation suggests that translational 417

inhibition acts on these genes to post-transcriptionally regulate their expression (Figure 6A). 418

Inhibited polysome loading of PhANGs (LHCB and Fed-1) was also observed in 3-(3,4-419

dichlorophenyl)-l,l-dimethylurea (DCMU)-treated dark-adapted tobacco plants during re-420

illumination or exposure to high light (Petracek et al., 1997), treatments that interfere with the 421

operational control of retrograde signaling. Taken together, these results and our findings 422

indicate that translational regulation of PhANG expression is employed by both the biogenic 423

control (PGE) and the operational control (redox and reactive oxygen species) exerted by 424

retrograde signaling. 425

Compared to repressed translation of RBCS genes and LHCA4, the translation of the two 426

ribosomal protein-encoding genes tested (PSRP5 and RPL4) was even enhanced under Lin 427



23

treatment (Figure 6B). Lin represses plastid translation (Mulo et al., 2003), including the 428

synthesis of all plastid-encoded subunits of the ribosome. One might have expected that, in order 429

to achieve coordination with the plastid-encoded subunits, cytosolic translation of the nucleus-430

encoded ribosomal subunits would also be repressed. The plastid-encoded proteins account for 431

~0.17% of the total cellular protein upon Lin treatment (Supplemental Figure S1A), indicating 432

that a basal level of translation still occurs. The observed up-regulated translation of nucleus-433

encoded ribosomal subunits simply could be a compensatory reaction that occurs in response to 434

the deficiency in plastid-encoded subunits, or alternatively, may prepare plastids that are blocked 435

in their development by Lin (mimicking an early stage of plastid development) for subsequent 436

enhancement of translation upon illumination. 437

A number of studies have suggested that translation and mRNA turnover are intimately 438

connected. For example, the slow turnover of polysome-loaded Fed-1 mRNA in the light was 439

hypothesized to be due to the destabilizing CAUU motif being hidden by translating ribosomes 440

(Dickey et al., 1994). A possible explanation for the less repressed transcript accumulation of 441

HiToP ribosomal protein genes could be that the up-regulated loading of the transcripts with 442

ribosomes prevents them from being degraded. Irrespective of the mechanism of transcript 443

stabilization, the encoded ribosomal proteins do not accumulate (Table 1) and cannot be detected 444

by immunoblot analysis (Figure 4B), indicating that they are epistatically regulated at the post-445

translational level, by protein degradation. Translational control provides more rapid changes in 446

cellular concentrations of proteins compared to transcriptional regulation and, therefore, may be 447

particularly important to mediate fast responses to environmental cues. Translational regulation 448

mostly occurs at the initiation stage of translation (Sonenberg and Hinnebusch, 2009). How the 449

cytosolic ribosome distinguishes between the different types of genes (PhANGs versus 450

ribosomal protein-encoding genes) to differentially regulate their translation, is currently 451

unknown. It seems reasonable to speculate that translational activator and/or repressor proteins 452

are involved that recognize specific features in the 5’ untranslated regions of the mRNAs. 453

GUN1 was suggested to regulate chloroplast proteostasis (Colombo et al., 2016; Tadini et 454

al., 2016; Llamas et al., 2017). By conducting a proteomic analysis, we identified 128 down-455

regulated and 14 over-accumulating chloroplast proteins in gun1 in comparison to the wild type 456

upon Lin treatment (Supplemental Table S2; Supplemental Dataset S2). By contrast, in the gun5 457

mutant, only 15 chloroplast proteins were identified as down-regulated and 6 as over-458



24

accumulated. Furthermore, among the 128 chloroplast proteins that were down-regulated in gun1, 459

a large proportion functions in different aspects of protein metabolism (Figure 1C). The reduced 460

accumulation of these proteins in gun1 indicates that they are possible targets of GUN1 action 461

and supports an important role of GUN1 in the control of plastid proteostasis. GUN1 was 462

reported to restore the accumulation of plastid ribosomal protein PRPS1 in gun1 prps1 and gun1 463

prps21 double mutants, regardless of unchanged PRPS1 transcript abundance (Tadini et al., 464

2016). We did not observe an over-accumulation of PRPS1 in gun1, neither under control 465

conditions nor upon treatment with Lin (Supplemental Table S2 and Supplemental Dataset S1). 466

We recently demonstrated that GUN1 controls plastid protein import when retrograde signaling 467

is affected either by genetic perturbations or by Lin or NF treatment (Wu et al., 2019). Although 468

the exact function of GUN1 in protein import remains to be determined, its interaction with the 469

cpHSC70-1 chaperone suggests that GUN1 may control the fate of newly imported proteins, in 470

that it promotes either folding into a functional protein or degradation by envelope-associated 471

Clp protease (Flores-Pérez et al., 2016). 472

The cytosolic UPS was demonstrated to degrade unimported chloroplast and 473

mitochondrial precursor proteins (preproteins; Lee et al., 2009; Wrobel et al., 2015; 474

Shanmugabalaji et al., 2018). The transcription factor GLK1 controls the expression of a large 475

number of PhANGs and participates in GUN1-mediated retrograde communication (Kakizaki et 476

al., 2009; Waters et al., 2009). It was shown that GLK1 is degraded by the UPS upon exposure to 477

Lin or NF (Tokumaru et al., 2017), suggesting involvement of the cytosolic UPS in the post-478

translational regulation of plastid proteostasis in retrograde signaling. GUN1 is required for 479

efficient plastid protein import under conditions that affect retrograde signaling (Wu et al., 2019). 480

Together, reduced protein import and compromised inhibition of translation would result in over-481

accumulation of preproteins in the cytosol of gun1 and activation of the cytosolic UPS (Wu et 482

al., 2019). In agreement with this model, the cytosolic chaperones HSP90.1, HSP70-2 and 483

HSP70-4 are strongly over-accumulated at the protein level in the gun1 clpc1 double mutant and 484

the gun1 single mutant upon Lin or NF treatment (Wu et al., 2019). Interestingly, transcriptional 485

up-regulation of these three HSPs was observed in gun1 also under control conditions 486

(Supplemental Table S3), while they do not over-accumulate at the protein level (Supplemental 487

Table S1; Wu et al., 2019). This finding suggests that the expression of these cytosolic 488

chaperones is controlled mainly by post-transcriptional mechanisms. 489



25

In summary, the data presented here demonstrate extensive post-transcriptional regulation 490

in the PGE pathway of plastid retrograde signaling and diverse cytosolic responses to plastid 491

translation inhibition. Our work has determined the extent of two post-transcriptional layers of 492

regulation in retrograde signaling: translational regulation (which is at least in part dependent on 493

GUN1) and regulation of protein stability (which is independent of GUN1). It will be interesting 494

to analyze other retrograde signaling pathways (e.g., the TPB pathway) to determine if these 495

regulatory mechanisms are conserved across all pathways. 496

497

498



26

MATERIALS AND METHODS 499

Plant Material and Growth Conditions 500

All experiments were performed with Arabidopsis (Arabidopsis thaliana) accession Columbia 501

(Col-0). The gun1-101 mutant used in this study was described previously (Wu et al., 2018). The 502

gun5-1 mutant (Mochizuki et al., 2001) was kindly provided by Dr. Bernhard Grimm (Humboldt 503

University, Berlin). For plant growth under aseptic conditions, seeds were surface-sterilized with 504

1.2% NaOCl (v/v) for 10 min, washed 5 times with sterile water and sown on 0.5× Murashige & 505

Skoog (MS) medium (Murashige and Skoog, 1962) containing 1% (w/v) sucrose in Petri dishes. 506

The seeds were stratified for 2 days in the dark at 4°C prior to germination. The seeds were first 507

incubated for 8 h in the light to promote germination and then grown in the dark for 5 days 508

followed by 2 days in continuous light. For Lin treatment, the Lin concentration in the medium 509

was 0.5 mM. 510

511

RNA Extraction, RT-qPCR and RNA Gel Blot Analyses 512

Total RNA was extracted with the NucleoSpin® RNA Plant kit (Macherey-Nagel) according to 513

the manufacturer’s instruction. To completely eliminate contaminating genomic DNA, a second 514

DNase digestion was performed with the TURBO DNA-free kit (Invitrogen). For northern blot 515

analysis, total RNA samples were separated in 1% (w/v) denaturing agarose gels (containing 516

formaldehyde), blotted onto Hybond-XL nylon membranes (GE Healthcare) and then cross-517

linked by UV light. Hybridization probes were generated by amplifying cDNA sequences with 518

gene-specific primers, followed by labeling with [α32P]dCTP with the Megaprime DNA labeling 519

system (GE Healthcare). Hybridizations were performed at 65oC overnight in Church buffer 520

(Church and Gilbert, 1984). The experiments were repeated two times with similar results. 521

Primers used for generation of hybridization probes are listed in Supplemental Table S4. 522

523

Mass Spectrometry and Label-Free Protein Quantification 524

For proteomic analysis of the wild type, gun1 and gun5 in control conditions or upon treatment 525

with Lin, seedlings were grown for 5 days in the dark followed by 2 days in continuous light 526

without (control) or with 0.5 mM Lin. Protein extraction and on-column digestion with trypsin 527

and mass spectrometric (MS) analyses were conducted essentially as described previously (Wu 528

et al., 2018). In brief, peptides were separated by EASY-nLC 1000 nanoflow HPLC (Proxeon 529



27

Biosystems, Odense, Denmark) using an C18 LC Column (Acclaim PepMap 100, 2 µm, 250 mm, 530

Thermo Scientific) with a 230 min linear gradient (4.25-51% v/v) of acetonitrile and a final 531

peptide elution step for 10 min with 76.5% (v/v) acetonitrile. A Q-Exactive Plus (Thermo Fisher 532

Scientific) high-resolution Orbitrap hybrid mass spectrometer was used and run in positive ion 533

mode. For full MS scans, the following settings were used: resolution: 70,000, automatic gain 534

control (AGC) target: 3E6, maximum injection time: 100 ms, scan range: 200−2000 m/z. For dd-535

MS2, the following settings were used: resolution: 175,000, AGC target: 1E5, maximum 536

injection time: 50 ms, loop count: 15, isolation window: 4.0 m/z, normalized collision energy 537

(NCE): 30. The following data-dependent settings were used: underfill ratio: 1%; apex trigger: 538

off; charge exclusion: unassigned, 1, 5, 5–8, >8; peptide match: preferred; exclude isotypes: on; 539

dynamic exclusion: 20.0 s. Protein identification and quantification was done with the MaxQuant 540

software (Version 1.5.8.3) and unique peptides were used for quantification. Post-data analysis 541

and statistical analysis were done with the Perseus software (Tyanova et al., 2016). For statistical 542

analysis, proteins that could be detected in at least two biological replicates of one genotype in at 543

least one condition were kept for further analysis. This resulted in 5558 proteins used for 544

downstream analysis and the missing values (i.e., proteins that could not be detected in some 545

samples/replicates) were imputed within the sample with a width of 0.3 (the Gaussian 546

distribution relative to the standard deviation of measured values) and downshift of 1.8 (units of 547

the standard deviation of the valid data) using the Perseus software to enable statistical analysis. 548

Proteins with a Student’s t test p value <0.05 and a fold change >2 were considered as 549

differentially expressed between genotypes or treatments. For mRNA (transcript) and protein co-550

analysis, the organelle-encoded genes were excluded, because oligo(dT) primer had been used 551

for reverse transcription in microarray sample preparation. For data visualization by scatter plots 552

(Figs. 2 and 3), averaged protein expression values were determined as follows: If there were 553

valid values (from detection by MS), the averaged protein expression values come from all valid 554

values. If there were no valid values (i.e., the protein was not detected in all three replicates in 555

the given condition or genotype), the protein expression values come from imputation. 556

557

Microarray Analysis 558

For whole genome microarray analysis, the wild type and gun1 were grown in control conditions 559

or treated with Lin as described above. After treatment with DNase, total RNA preparations were 560



28

further purified with the peqGOLD Optipure regent (PEQLAB) to remove polysaccharide 561

contaminations. The purified RNA samples were subjected to a quality check by denaturing 562

RNA gel electrophoresis and assayed in the Agilent 2100 bioanalyzer with the Agilent RNA 563

6000 Nano Kit (Agilent). Antisense cRNA synthesis and labeling were carried out according to 564

the manufacturer’s instruction (Affymetrix, Santa Clara, CA, US). Labeled antisense cRNA 565

samples were hybridized to Affymetrix Arabidopsis Gene 1.0 ST Arrays (Affymetrix). 566

Hybridization, washing and scanning were conducted as described in the Affymetrix technical 567

manual. The raw data were analyzed and normalized at the gene level with the RMA algorithm 568

of the Expression Console v1.3 (Affymetrix). Two-way analysis of variance (ANOVA) was 569

used to identify differentially expressed genes. The Benjamini & Hochberg algorithm was used 570

to control the false discovery rate (FDR) of multiple tests in R (http://www.r-project.org/). 571

Subsequently, pairwise comparisons between genotypes and conditions were conducted by 572

Tukey HSD tests (using the “TukeyHSD” function in R). Genes with an FDR-adjusted p-value 573

<0.05 and fold change >2 were identified as differentially expressed genes. 574

575

Protein Extraction and Western Blot Analyses 576

Total cellular protein was extracted with a phenol-based method (Cahoon et al., 1992) and 577

quantified with the Pierce BCA Protein Assay Kit (Thermo Fisher Scientific) according to the 578

manufacturer’s instruction. Protein samples were separated by SDS-polyacrylamide gel (15% 579

w/v) electrophoresis (SDS-PAGE) and blotted onto PVDF membranes. Immunoblot detection 580

was performed using the enhanced chemiluminescence system (GE Healthcare) with specific 581

antibodies. Signals were detected with the G:box Chemi Imaging System (Syngene). Antibodies 582

were obtained from commercial suppliers (actin from Sigma; LHCA4, LHCB1, RBCS, RPL4 583

and cpHSC70 from Agrisera). The experiments were repeated two times with similar results. 584

585

Polysome Analyses 586

For isolation of polysomes, plants were germinated and grown under control conditions or 587

treated with Lin exactly as described for the microarray and proteomic experiments. Polysome 588

isolation and control treatments with puromycin were performed essentially as described (Barkan, 589

1998; Wu et al., 2018). Aliquots of 5 µL per fraction were analyzed by northern blotting as 590

described above. The experiments were repeated two times with similar results. 591



29

592

Statistical Analysis 593

To identify genes with significantly altered expression in microarray experiments, two-way 594

ANOVA was performed with the Benjamini & Hochberg algorithm to control the false discovery 595

rate (FDR) of multiple tests. The post pairwise comparisons between genotypes and conditions 596

were done by Tukey HSD tests. For proteomic analysis to identify differentially accumulated 597

proteins, two-tailed unpaired Student’s t test was used when a pair of conditions/genotypes 598

was compared. 599

600

Data Availability 601

The mass spectrometry proteomics data have been deposited to the ProteomeXchange 602

Consortium via the PRIDE partner repository with the dataset identifier PXD011759. The 603

microarray data have been deposited in Gene Expression Omnibus under the accession number 604

GSE122667. 605

606

Accession Numbers 607

The sequence data from this article can be found in the Arabidopsis Information Resource or 608

GeneBank/EMBL database under the following accession numbers: GUN1 (AT2G31400), 609

GUN5 (AT5G13630), PSRP5 (AT3G56910), RPL4 (AT1G07320), CA1 (AT3G01500), LOX2 610

(AT3G45140), PsaG (AT1G55670), PsaL (AT4G12800), PsaD (AT4G02770), CaSR 611

(AT5G23060), rbcL (ATCG00490), RBCS1A (AT1G67090), RBCS1B (AT5G38430), RBCS2B 612

(AT5G38420), RBCS3B (AT5G38410), LHCA1 (AT3G54890), LHCA2 (AT3G61470), LHCA3 613

(AT1G61520), LHCA4 (AT3G47470), LHCA5 (AT1G45474), LHCA6 (AT1G19150), LHCB1.1 614

(AT1G29920), LHCB1.2 (AT1G29910), LHCB1.3 (AT1G29930), LHCB1.4 (AT2G34430), 615

LHCB1.5 (AT2G34420), LHCB2.1 (AT2G05100), LHCB2.2 (AT2G05070), LHCB2.3 616

(AT3G27690), LHCB3 (AT5G54270), LHCB4.1 (AT5G01530), LHCB4.2 (AT3G08940), 617

LHCB4.3 (AT2G40100), LHCB5 (AT4G10340), LHCB6 (AT1G15820), NAD9 (ATMG00070), 618

NAD5B (ATMG00665), NAD1A (ATMG01275), NAD2B (ATMG01320), NAD7 (ATMG00510), 619

COX2 (ATMG00160), ORF25 (ATMG00640), COB (ATMG00220), RPS3 (ATMG00090), 620

621



30

SUPPLEMENTAL DATA 622

Supplemental Figure S1. Lin specifically represses plastid protein synthesis. 623

Supplemental Figure S2. The expression of LIPOXYGENASE 2 (LOX2) is repressed in both 624

the wild type and gun1 upon Lin treatment. 625

Supplemental Figure S3. Expression of LHCA, LHCB and RBCS genes in response to Lin 626

treatment in the wild type and the gun1-101 mutant. 627

Supplemental Figure S4. Puromycin-treated controls for the polysome profiles of LHCA4, 628

RBCS, PSRP5 and RPL4 in the wild type shown in Figure 6. 629

Supplemental Figure S5. Puromycin-treated controls for the polysome profiles of LHCA4, 630

RBCS, PSRP5 and RPL4 in gun1 shown in Figure 7. 631

Supplemental Table S1. Differentially expressed proteins in gun1 compared to the wild type 632

under control conditions. 633

Supplemental Table S2. Plastid-localized proteins that over-accumulate in gun1 relative to 634

the wild type upon Lin treatment. 635

Supplemental Table S3. Differentially expressed genes identified by microarray analysis in 636

gun1 compared to the wild type under control conditions. 637

Supplemental Table S4. List of oligonucleotides used in this study. 638

Supplemental Dataset S1. Mass spectrometry data of proteomic analyses of the wild type, 639

the gun1 mutant and the gun5 mutant under control conditions and under Lin treatment, and 640

significantly differentially expressed proteins identified between the wild type and the mutants. 641

Supplementary Dataset S2. The 128 plastid-localized proteins that accumulate to lower 642

levels in gun1 compared to the wild type (WT) under Lin treatment (log2 643

WT_Lin/gun1_Lin >1) and their response to Lin treatment (control/Lin). 644

Supplemental Dataset S3. Data used for scatter plots in Figures 2 and 3. 645

Supplemental Dataset S4. Differentially expressed genes between the wild type and the gun1 646

mutant under Lin treatment identified by microarray analysis. 647

Supplemental Dataset S5. HiToP genes identified in the wild type and gun1. 648

649

ACKNOWLEDGEMENTS 650



31

We are grateful to Dr. Bernhard Grimm (Humboldt University Berlin) for gun5-1 mutant seeds. 651

This research was financed by the Max Planck Society and a grant from the Deutsche 652

Forschungsgemeinschaft to R.B. (SFB TR175). 653

654



32

Table 1. Type I HiToP genes encoding plastid-localized proteins. Genes identified in the wild 655

type as log2 Control/Lin >4 at the protein level, but -1< log2 Control/Lin <1 at the mRNA level 656

are listed. The super-ratio (SR) was calculated as protein fold change divided by mRNA fold 657

change. The corresponding values in the gun1 mutant are included for comparison. The data 658

represent averages from three biological replicates. C/L: control/Lin; Chl syn: chlorophyll 659

synthesis; NDH: NAD(P)H dehydrogenase. 660

661

mRNA log2 C/L

Protein log2 C/L log2 SR

Locus Gene Function WT gun1 WT gun1 WT gun1

AT4G32260 ATPase, F0 complex, subunit B/B' ATPase 0.95 0.10 7.38 9.17 6.43 9.07

AT5G14320 Ribosomal protein S13/S18 family Translation 0.65 -0.15 6.50 8.07 5.85 8.22

AT4G25080 CHLM Chl syn 0.82 -0.08 6.49 6.03 5.67 6.10

AT3G56910 PSRP5 Translation 0.53 -0.19 6.42 7.14 5.89 7.33

AT1G67090 RBCS1A RBCS 0.27 -0.05 6.27 7.26 6.00 7.31

AT1G79040 PsbR PSII 0.74 0.09 6.24 5.96 5.51 5.87

AT3G55330 PsbP-like protein 1 (PPL1) PSII 0.93 0.22 6.07 5.49 5.14 5.27

AT5G54190 PORA Chl syn 0.30 0.19 6.04 0.75 5.73 0.56

AT2G05620 PGR5 PSI 0.92 -0.49 5.75 6.07 4.84 6.56

AT3G27160 RPS21/GHS1 Translation 0.82 -0.08 5.42 5.48 4.60 5.56

AT5G17870 PSRP6 Translation 0.79 -0.13 5.41 3.33 4.62 3.46

AT2G21960 metalloendopeptidase proteostasis 0.30 0.09 5.38 5.49 5.08 5.40

AT1G64770 NDH45 NDH 0.63 0.39 5.25 4.96 4.61 4.57

AT3G63540 PsbP family protein PSII 0.34 -0.06 5.23 5.84 4.89 5.89

AT5G48220 Aldolase-type TIM barrel family – 0.55 0.24 4.97 4.10 4.43 3.86

AT3G54210 RPL17 Translation 1.00 -0.40 4.90 5.09 3.90 5.49

AT5G40950 RPL27 Translation 0.90 -0.17 4.85 6.45 3.95 6.62

AT3G15190 RPS20 Translation 0.87 0.18 4.83 5.53 3.96 5.34

AT1G16720 HCF173 Translation 0.05 -0.31 4.83 4.91 4.79 5.22

AT2G26340 hypothetical protein – 0.65 -0.56 4.73 4.03 4.09 4.59

AT5G02830 TPR superfamily protein – 0.41 0.29 4.30 4.34 3.89 4.05

AT4G23890 NDHS/CRR31 NDH 0.84 0.01 4.28 4.02 3.45 4.01



33

AT4G18370 DEG5 proteostasis 0.74 0.17 4.24 3.28 3.50 3.12

AT5G11450 PsbP domain protein (PPD5) PSII 0.82 -0.21 4.20 3.13 3.38 3.33

662

663



34

FIGURE LEGENDS 664

665

Figure 1. GUN1 regulates plastid proteostasis in the plastid gene expression (PGE) pathway of 666

retrograde signaling. 667

A, Volcano plots depicting the protein accumulation in gun1 and gun5 compared to the wild type 668

(WT) in control conditions and upon Lin treatment. Proteins with a P-value <0.05 (Student’s t-669

test), and a log2 value of the ratio WT/mutant > 1 or < -1 are shown in blue and red, respectively. 670

B, Histograms showing the subcellular localization of proteins that are differentially expressed in 671

gun1 or gun5 compared to the wild type in control conditions and upon Lin treatment. The 672

numbers above the bars indicate the number of proteins identified as being differentially 673

expressed between mutant and the wild type. The number of plastid-localized proteins is 674

indicated in the green part of each bar. pt: plastid, cy: cytosol, ER: endoplasmic reticulum, ex: 675

extracellular, mt: mitochondrion, nu: nucleus, per: peroxisome, PM: plasma membrane, vac: 676

vacuole, Golgi: Golgi apparatus. C, Histogram illustrating the functional categories of 677

chloroplast proteins that are potentially involved in plastid proteostasis and accumulate less in 678

gun1 compared to the wild type upon Lin treatment. 679

680

Figure 2. Transcript and protein co-analysis reveals extensive translational and post-translational 681

regulation in retrograde signaling. 682

A,B, Scatter plots showing the high correlation of gene regulation at the protein level (B) 683

compared to the transcript (mRNA) level (A) between the gun1 mutant and the wild type (WT) 684

in response to Lin treatment. All nucleus-encoded genes whose protein products can be detected 685

by mass spectrometry (in total 5449 genes; for details see Methods) were included in the analysis. 686

The fold changes in the Lin treatment relative to the untreated control (log2; averaged from three 687

biological replicates) were compared between gun1 and the wild type to calculate the Pearson 688

correlation coefficient (R) and the P-value (P). Red triangle: LOX2 gene. 689

690

Figure 3. HiToP genes identified. 691

A,B, Scatter plots to compare the correlation of regulation between transcripts and proteins in 692

control conditions versus Lin treatment in the wild type (A) and the gun1 mutant (B). The HiToP 693

genes were classified into two types. Type I: log2 protein control/Lin >3 or <-3, and -1< log2 694



35

mRNA control/Lin <1 (green and red dashed boxes); type II: log2 mRNA control/Lin >1 or <-1, 695

but log2 super-ratio of protein fold change to mRNA fold change of control to Lin treatment >3 696

or <-3 (highlighted as red dots, purple dots and blue triangles). Selected genes of special interest 697

are marked: green dots: LHCB1.4; blue dots: CA1; purple dots: RBCS1B and RBCS3B (also 698

identified as type II HiToP genes in the wild type); blue triangles: other examples of genes that 699

were identified as type II HiToP genes in the wild type, but as type I HiToP genes in gun1 (PsaG, 700

PsaL, PsaD, and CaSR). See text for details. C, Up- and down-regulated HiToP genes identified 701

in the wild type (WT) and the gun1 mutant. The numbers in the bars give the numbers of genes 702

identified in each group. The insets show the number of HiToP genes that are down-regulated at 703

the protein level upon Lin treatment and whose products are localized in chloroplasts (chl) or 704

outside of chloroplasts (non). D, Pie chart illustrating the functional categories of the 108 plastid-705

localized HiToP proteins that are down-regulated in the wild type at the protein level upon Lin 706

treatment. The numbers give the total number of genes identified in each functional category, 707

while the numbers in parenthesis denote the number of type I HiToP genes. The genes related to 708

translation and proteostasis are separated out. E, Venn diagram illustrating the overlap of down-709

regulated type I genes (green box in panels A and B) between the wild type and the gun1 mutant. 710

Green numbers indicate the number of genes whose protein products localize to plastids. F, Gene 711

Ontology (GO) enrichment of cellular component analysis of the 182 plastid-localized down-712

regulated type I HiToP genes in gun1. The 5449 proteins identified by MS were used as 713

reference list (ref.list) for GO terms of enrichment analysis (http://www.pantherdb.org/). The 714

fold enrichment was calculated by binomial test using the Bonferroni correction for multiple 715

testing. The column ‘No. in ref. list’ indicates the number of genes in each GO term among the 716

5449 reference genes. The columns ‘Expected’ and ‘Identified’ indicate the number of genes that 717

were expected or identified for each GO term within the 182 plastid-localized down-regulated 718

type I HiToP genes. 719

720

Figure 4. Northern blot and western blot analyses to reveal the regulation of different type of 721

HiToP genes. 722

A, Northern blot analysis of selected HiToP genes. Unlike LHCB1 (the probe used does not 723

distinguish between different isoforms of LHCB1) whose transcript accumulation is largely 724

repressed by Lin treatment in the wild type, the transcripts of LHCA4 and RBCS (the probe used 725



36

does not distinguish between different isoforms of RBCS) are less repressed and the RPL4 726

transcripts are nearly unchanged. Seeds from the wild type and gun1 were germinated and grown 727

for 5 days in the dark followed by 2 days in continuous light in the absence (control) or presence 728

of 0.5 mM Lin. Methylene blue staining of rRNAs after blotting was performed as loading 729

control. B, At the protein level, LHCA4, RBCS and RPL4 are all below the detection limit of 730

immunoblots both in the wild type and gun1 under Lin treatment. For LHCB1 in Lin treatment, 731

faint bands can be detected in gun1, but not in the wild type. Actin and the chloroplast chaperone 732

protein cpHSC70 were included as loading controls. 733

734

Figure 5. Polysome profiles demonstrate that translation of LHCB is repressed in gun1 upon Lin 735

treatment. In the wild type, transcript accumulation of LHCB1 (the probe used does not 736

distinguish between different isoforms of LHCB1) is dramatically reduced under Lin treatment 737

(see also Figure 4A). In gun1, translation of LHCB1 is down-regulated upon Lin treatment, as 738

evidenced by the distribution of LHCB1 transcripts in polysome fractions 9-11 (boxed). 739

Puromycin-treated control samples were included to identify the polysome-containing gradient 740

fractions. Puromycin releases ribosomes from the mRNA. The wild type and gun1-101 were 741

grown in the presence (Lin) or absence (Control) of Lin in the dark for 5 days prior to 2 days in 742

continuous light. The wedges above the blots indicate the increasing sucrose concentration 743

across the gradient. The ethidium bromide-stained rRNAs in the gels prior to blotting are also 744

shown. 745

746

Figure 6. Polysome profiles uncover different modes of regulation of PhANGs and ribosomal 747

protein-encoding HiToP genes. 748

A, Comparison of polysome profiles under Lin treatment to those of the untreated control 749

demonstrates the strong translation inhibition of RBCS and LHCA4 (HiToP PhANGs) in 750

response to plastid translation inhibition in the wild type. The probe used does not distinguish 751

between different isoforms of RBCS. The three major polysome-containing fractions are boxed. 752

The wedges above the blots indicate the increasing sucrose concentration across the gradient. B, 753

Polysome profiles for nuclear genes encoding plastid ribosomal proteins (PSRP5 and RPL4) 754

indicate that their translation is up-regulated in response to Lin treatment. The three major 755

polysome-containing fractions are boxed for both mRNAs. See Supplemental Figure S4 for 756



37

puromycin controls. The ethidium bromide-stained rRNAs in the gels prior to blotting are also 757

shown. 758

759

Figure 7. Translational regulation in the plastid gene expression (PGE) pathway of retrograde 760

signaling needs the action of GUN1. 761

A, Comparison of the polysome profiles upon Lin treatment with those of the untreated controls 762

for RBCS and LHCA4 demonstrates that translational inhibition of HiToP PhANGs in gun1 in 763

response to Lin treatment is compromised. The probe used does not distinguish between different 764

isoforms of RBCS. B, Comparison of polysome profiles upon Lin treatment with those of the 765

untreated controls for PSRP5 and RPL4 demonstrates that up-regulation of their translation in 766

response to Lin treatment is compromised in gun1 (in that the shift to heavier gradient fractions 767

does not occur; cf. Figure 6). In A and B, the three major polysome-containing fractions are 768

boxed. The wedges above the blots indicate the increasing sucrose concentration across the 769

gradient. The ethidium bromide-stained rRNAs in the gels prior to blotting are also shown. See 770

Supplemental Figure S5 for puromycin controls. 771

772



38

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https://www.ncbi.nlm.nih.gov/pubmed?term=Esteves P%2C Pecqueur C%2C Ransy C%2C Esnous C%2C Lenoir V%2C Bouillaud F%2C Bulteau AL%2C Lombes A%2C Prip%2DBuus C%2C Ricquier D%2C Alves%2DGuerra MC %282014%29 Mitochondrial retrograde signaling mediated by UCP2 inhibits cancer cell proliferation and tumorigenesis%2E Cancer Res&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Mochizuki N%2C Brusslan JA%2C Larkin R%2C Nagatani A%2C Chory J %282001%29 Arabidopsis genomes uncoupled 5 %28GUN5%29 mutant reveals the involvement of Mg%2Dchelatase H subunit in plastid%2Dto%2Dnucleus signal transduction%2E Proc Natl Acad Sci U S A&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Murashige T%2C Skoog F %281962%29 A revised medium for rapid growth and bio assays with tobacco tissue cultures%2E Physiol Plant&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Woodson JD%2C Perez%2DRuiz JM%2C Schmitz RJ%2C Ecker JR%2C Chory J %282013%29 Sigma factor%2Dmediated plastid retrograde signals control nuclear gene expression%2E Plant J&dopt=abstract


https://scholar.google.com/scholar?as_q=Sigma factor-mediated plastid retrograde signals control nuclear gene expression&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

https://scholar.google.com/scholar?as_q=Sigma factor-mediated plastid retrograde signals control nuclear gene expression&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Woodson&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wrobel L%2C Topf U%2C Bragoszewski P%2C Wiese S%2C Sztolsztener ME%2C Oeljeklaus S%2C Varabyova A%2C Lirski M%2C Chroscicki P%2C Mroczek S%2C Januszewicz E%2C Dziembowski A%2C Koblowska M%2C Warscheid B%2C Chacinska A %282015%29 Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol%2E Nature&dopt=abstract

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https://scholar.google.com/scholar?as_q=Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol&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

https://scholar.google.com/scholar?as_q=Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wrobel&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wu GZ%2C Chalvin C%2C Hoelscher MP%2C Meyer EH%2C Wu XN%2C Bock R %282018%29 Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED 1%2E Plant Physiol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED 1&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

https://scholar.google.com/scholar?as_q=Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED 1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2018&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Wu GZ%2C Meyer EH%2C Richter A%2C Schuster M%2C Ling QH%2C Sch�ttler MA%2C Walther D%2C Zoschke R%2C Grimm B%2C Jarvis P%2C Bock R %282019%29 Control of Retrograde Signaling by Protein Import and Cytosolic Folding Stress%2E Nat Plants&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Control of Retrograde Signaling by Protein Import and Cytosolic Folding 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

https://scholar.google.com/scholar?as_q=Control of Retrograde Signaling by Protein Import and Cytosolic Folding Stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wu&as_ylo=2019&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Xiao YM%2C Savchenko T%2C Baidoo EEK%2C Chehab WE%2C Hayden DM%2C Tolstikov V%2C Corwin JA%2C Kliebenstein DJ%2C Keasling JD%2C Dehesh K %282012%29 Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress%2Dresponse genes%2E Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes&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

https://scholar.google.com/scholar?as_q=Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xiao&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Yasumura Y%2C Moylan EC%2C Langdale JA %282005%29 A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land plants%2E Plant Cell&dopt=abstract

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

https://scholar.google.com/scholar?as_q=A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land 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

https://scholar.google.com/scholar?as_q=A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yasumura&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1


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