retrograde signals navigate the path to chloroplast …...mutations in sig2, sig6 and prin2...

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Update Review for Focus Issue, Energy: Light and Oxygen Dynamics 1

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Retrograde signals navigate the path to chloroplast development 3

Tamara Hernández-Verdeja and Åsa Strand* 4

Umeå Plant Science Centre, Dept. of Plant Physiology, Umeå University, SE-901 87 Umeå, 5

Sweden. 6

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*Corresponding author: 8

Åsa Strand 9

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, S-901 87 10

Umeå, Sweden 11

Phone: +46 90 786 9314 12

Email: [email protected] 13

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Key words: 15

Chloroplast, seedling development, retrograde, photosynthesis, signalling, GUN1 16

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This work was supported by grants from the Swedish research foundation, VR (ÅS). 18

Å.S. and T.H.V. contributed equally to writing of the manuscript. 19

Summary: Complex signalling networks between the chloroplast and the nucleus mediate the 20

emergence of the seedling into the light and the establishment of photosynthesis. 21

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1. INTRODUCTION 24

Light is the main source of energy for life on Earth, and plants and algae are able to convert 25

light energy, through photosynthesis, into chemical energy that can be used by all organisms. 26

The photosynthetic reactions are housed in the chloroplasts but the chloroplasts are also the site 27

for synthesis of essential compounds like fatty acids, vitamins, amino acids and tetrapyrroles. 28

Given their essential role, the correct formation and function of chloroplasts is vital for the 29

growth and development of plants and algae, and hence for almost all organisms. Chloroplasts 30

evolved from an endosymbiotic event where a photosynthetic prokaryotic organism was 31

acquired by a pro-eukaryotic cell. With time, the photosynthetic prokaryote lost or transferred 32

most of its genes to the host genome. As a result, plastid protein complexes, such as the 33

photosynthetic complexes, are encoded by genes of both the nuclear and plastid genomes. This 34

Plant Physiology Preview. Published on December 18, 2017, as DOI:10.1104/pp.17.01299

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division of genetic information requires a precise co-ordination between the two genomes to 35

achieve proper plastid development and function. Plastid development and gene expression is 36

under nuclear control, in what is referred to as anterograde control. However, there is also a 37

signalling system originating in the plastids, so called retrograde signals, transmitting 38

information about the developmental and functional state of the plastids to the nucleus to 39

regulate nuclear gene expression. Retrograde signalling is a complex network of signals that can 40

be divided into ‘biogenic control’, referring to signals generated by the plastid as it develops 41

from a proplastid or etioplast into a chloroplast, and ‘operational control’ signals, including 42

those generated from a mature chloroplast in response to environmental perturbations (Chan et 43

al., 2016). 44

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2. FROM THE PLASTID SIGNAL TO THE COMPLEX NETWORK OF PLASTID-TO-46

NUCLEUS SIGNALLING 47

The original idea of a single plastid signal has evolved over the years and we now know that the 48

retrograde signalling system is a complex network of signals and pathways, most of which are 49

still unknown. To date, four major signals/pathways have been described: (1) signals related to 50

the tetrapyrrole biosynthesis pathway (TBP), (2) signals triggered by plastid gene expression 51

(PGE), (3) reactive oxygen species (ROS) and changes to the activity of the photosynthetic 52

electron transport chain (PET), and (4) signals deriving from disturbed plastid metabolism such 53

as accumulation of 3’-phosphoadenosine 5’-phosphate (PAP), 2-C-methyl-D-erythritol 2,4-54

cyclodiphosphate (MEcPP), or carotenoid derivatives like β-cyclocitral or apocarotenoids 55

(Estavillo et al., 2011; Ramel et al., 2012; Xiao et al., 2012; Avendaño-Vázquez et al., 2014). 56

The signals derived from plastid metabolism are mostly related to stress responses and 57

operational control of the chloroplast. Those pathways have recently been extensively reviewed, 58

and will not be covered in this review (Bobik and Burch-Smith, 2015; Chi et al., 2015; De 59

Souza et al., 2017). Our focus here is on biogenic control and the retrograde signals linked to 60

the early light response and to chloroplast development. 61

62

The biogenic signals can be linked to the tetrapyrrole biosynthesis pathway (TBP), plastid gene 63

expression (PGE) and changes to the photosynthetic electron transport activity (Fig. 1). 64

Chlorophyll and the other major tetrapyrroles, like heme, siroheme, and phytochromobilin, 65

derive from a common biosynthetic pathway (TBP) located in the plastids. Arabidopsis mutants 66

with impaired communication between the chloroplast and the nucleus, referred to as the gun 67

(genomes uncoupled) mutants were isolated from forward genetic screens (Susek et al., 1993; 68

Mochizuki et al., 2001; Woodson et al., 2011). GUN2-6 all encode components closely 69

associated with tetrapyrrole biosynthesis and the respective mutants have changes to the flux 70



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through TBP (Details Box 1). The phenotype of the gun mutants has been linked to oxidative 71

stress causing perturbations of flux through the TBP resulting in accumulation of both ROS and 72

specific metabolites (reviewed in Larkin, 2016). In addition, the tetrapyrrole heme has been 73

proposed as a plastid signal positively regulating the expression of Photosynthesis Associated 74

Nuclear Genes (PhANGs) during chloroplast development (Woodson et al., 2011). During 75

chloroplast development, precise co-ordination between the synthesis of the light absorbing 76

pigments and the expression of the nuclear-encoded chlorophyll-binding proteins is required to 77

correctly assemble the antennae-reaction centre super complexes of PSII and PSI. Thus, 78

regulation of PhANG expression is linked to tetrapyrrole biosynthesis and it has been suggested 79

that PhANG expression is controlled by a balance between light signalling pathways and a 80

plastid signal triggered by impaired flux through chlorophyll biosynthesis, Mg-ProtoIX and or 81

heme (Woodson et al., 2011; Barajas-López et al., 2013). Furthermore 1O2, a known operational 82

control signal, has been proposed to also play a role during chloroplast development by 83

repressing PhANGs in response to moderate increases of chlorophyll precursors (Page et al., 84

2017b). 85

86

The status of plastid transcription and translation as a trigger for a retrograde signal has been 87

demonstrated by repression of PhANG expression following chemical treatments such as the 88

plastid translational inhibitors lincomycin or rifampicin, which selectively inhibits the plastid-89

encoded RNA polymerase (PEP) (Woodson et al., 2013; Chan et al., 2016). The repression of 90

PhANG expression phenotype was also observed in mutants affected in the plastid 91

transcriptional machinery, including: the RpoTp/SCA3 protein of the nuclear-encoded RNA 92

polymerase (NEP); the sigma factors SIG2 and SIG6 essential for PEP activity; and other 93

proteins required for full expression of the PEP-dependent genes like Polymerase-Associated 94

Protein7 (PAP7), Plastid Redox Insensitive2 (PRIN2) or Yellow Seedlings1 (YS1) (Hricová et 95

al., 2006; Gao et al., 2011; Kindgren et al., 2012; Woodson et al., 2013) (Details Box 2). The 96

exact nature of the signal generated by PGE is unknown and different but overlapping pathways 97

have been suggested (Woodson et al., 2013). One of the proposed signalling pathways involves 98

PEP-transcribed tRNAGlu, the starting and limiting substrate of TBP, thus, linking PGE to TBP-99

mediated signalling with the regulation of PhANG expression during chloroplast biogenesis 100

(Woodson et al., 2013). 101

102

In the mature chloroplast, ROS generated by photosynthesis and changes to the redox state of 103

PET act as indicators of environmental fluctuations, and generate signals in the context of 104

operational control (Chan et al., 2016). However, there are also reports where an imbalance of 105

PET is perceived in the frame of biogenic control during the initial stages of plastid 106



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development. IMMUTANS (IM) encodes a plastid terminal oxidase (PTOX) required for 107

chloroplast biogenesis, both in seedlings and in adult leaves. PTOX functions as a versatile 108

plastoquinol terminal oxidase in plastid membranes, transferring electrons from the 109

plastoquinone (PQ) pool to molecular oxygen. IM is a component of a redox pathway that 110

desaturates phytoene, where electrons are transferred from phytoene to PQ via phytoene 111

desaturase, and from PQ to oxygen via IM. Thus, in the ptox mutant this pathway is inhibited 112

and carotene biosynthesis is blocked at the phytoene desaturase step. The lack of protective 113

carotenoids results in photo-oxidation of plastid components, which halts plastid development 114

(Kambakam et al., 2016; Pogorelko et al., 2016). Transcriptomic analyses of etiolated and de-115

etiolating im seedlings revealed altered expression of nuclear transcription factors that control 116

PhANG expression (Kambakam et al., 2016). The retrograde signal or signals triggered by the 117

imbalance of PET during chloroplast development could potentially coordinate chlorophyll with 118

carotenoid biosynthesis during the early light response. 119

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3. FROM THE CHLOROPLAST TO THE NUCLEUS: TRANSDUCERS OF PLASTID 122

SIGNALS 123

The different signals originating in the plastids need to be transduced to the nucleus and 124

connected to transcriptional regulators that control the transcription of PhANGs. GENOMES 125

UNCOUPLED1 (GUN1) seems to act as a central hub in the chloroplast, integrating different 126

retrograde signals. Similar to GUN5, GUN1 plays a role in the tetrapyrrole-mediated pathway 127

(Koussevitzky et al., 2007) and genetic analyses revealed that GUN1 is also implicated in the 128

PGE-triggered retrograde signal, as supported by the gun1 mutation reverting the altered 129

PhANG expression phenotype caused by mutations in SIG2, SIG6 and PRIN2 (Kindgren et al., 130

2012; Woodson et al., 2013). GUN1 is a nuclear-encoded, plastid-localized protein with 131

homology to pentatricopeptide repeat (PPR) domain-containing proteins but the exact molecular 132

role(s) of GUN1 remains unknown. PPR proteins are involved in RNA processing and initially a 133

fragment of GUN1 including the PPR domain was shown to bind DNA. However, no 134

interaction was detected between GUN1 and nucleic acids when the entire GUN1 protein was 135

used (Koussevitzky et al., 2007; Tadini et al., 2016). Proteomic analyses have identified a large 136

number of GUN1-interacting proteins representing a wide range of functions, including 137

ribosomal proteins and factors involved in ribosome biogenesis, enzymes in tetrapyrrole 138

biosynthesis, and protein chaperones involved in protein import to the chloroplast, assembly of 139

proteins and protein degradation (Tadini et al., 2016). However, the identified interactions were 140

weak, suggesting that GUN1 could transiently associate with different protein complexes 141

(Tadini et al., 2016). In addition, given the diversity of proteins identified, the proteomic efforts 142



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have so far generated few clues about the true function(s) of GUN1. Possibly, in vivo interaction 143

studies would generate more relevant results. 144

145

A plant homeodomain transcription factor with transmembrane domains located to the 146

chloroplast envelope, named PTM, was identified as a potential transduction component of the 147

GUN1-mediated signalling pathway (Sun et al., 2011). Following treatments with lincomycin or 148

NF a truncated form of PTM (N-PTM) accumulated in the nucleus in a serine protease-149

dependent manner. Furthermore, the cleaved N-PTM form was shown to directly control the 150

expression of transcription factors, such as Abscisic Acid Insensitive4 (ABI4), in the nucleus 151

(Sun et al., 2011). The gun phenotype of the ptm mutant was recently challenged after analysis 152

of three ptm mutant alleles (Page et al., 2017a), and alternative pathways for the transduction of 153

the plastid signal to the nucleus were suggested. An alternative for the control of ABI4 activity 154

in response to a retrograde signal is a calcium-dependent, three-component mitogen-activated 155

protein kinase (MAPK) system. Perturbations of chloroplast function, following NF and/or 156

lincomycin treatments, cause transient increases in cytosolic Ca2+ that activates the MAPK 157

cascade involving the calcium-binding protein 14-3-3. The activated MPK3 or MPK6 158

phosphorylates and activates ABI4 in the nucleus (Guo et al., 2016). In addition, an as yet-159

unknown mechanism transduces retrograde signals to control the protein levels of the nuclear 160

transcription factor Golden2-like1 (GLK1), in a GUN1-independent way (Tokumaru et al., 161

2017). 162

163

Overall, very few transcriptional regulators have been assigned a role in retrograde signalling 164

during the process of chloroplast development. ABI4 acts downstream of GUN1 and the 165

calcium signal, and in response to chloroplast dysfunction the GUN1-PTM module activates the 166

transcription of ABI4, whereas the Ca2+-activated MPK3/MPK6 phosphorylates ABI4 which 167

will then bind the promoters of PhANGs, repressing their transcription (Koussevitzky et al., 168

2007; Sun et al., 2011; Guo et al., 2016). The GLK1 and GLK2 transcription factors are major 169

players in chloroplast biogenesis, integrating retrograde and light signals (Waters et al., 2009; 170

Martín et al., 2016). GLK1 and GLK2 promote chloroplast development by directly activating 171

the expression of nuclear genes encoding proteins involved in chlorophyll biosynthesis, light 172

harvesting, and electron transport (Waters et al., 2009). The important role of the GLKs is 173

reinforced by the pale glk1glk2 double mutant with partially developed chloroplasts and a, albeit 174

weak, gun phenotype (Fitter et al., 2002; Waters et al., 2009). Although genetic analyses 175

indicated that GLK1 and GLK2 are redundant, recent work has revealed specificity that is 176

regulated at transcriptional and post-transcriptional levels (Powell et al., 2012; Kobayashi et al., 177

2013; Wang et al., 2013; Martín et al., 2016; Tokumaru et al., 2017). 178

179



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4. INTERACTION OF PLASTID AND LIGHT SIGNALS DURING CHLOROPLAST 180

DEVELOPMENT 181

Chloroplast biogenesis is a complex process and the mechanisms involved differ not only 182

between different plant species but also between different organs within the individual plant. 183

Numerous studies have revealed the significance of proper chloroplast development during all 184

stages of plant growth and the necessity for co-ordination between growth and chloroplast 185

development (Pogson et al., 2015; Chan et al., 2016). Much of our current knowledge of the 186

molecular mechanisms controlling chloroplast biogenesis comes from studies using the 187

angiosperm model species Arabidopsis thaliana. Angiosperms germinate in darkness (e.g. 188

covered by soil) and develop following a dark-adapted program named skotomorphogenesis, 189

which is characterized by long hypocotyls and etiolated cotyledons that contain a form of 190

plastid referred to as etioplasts. Following light exposure, the developmental program changes 191

into photomorphogenesis, hypocotyl elongation is inhibited and the cotyledons turn green and 192

develop functional chloroplasts (Pogson et al., 2015). In adult leaves, mature chloroplasts 193

develop from proplastids in the stem cells of the apical meristem. Proplastids start to 194

differentiate and form the first extended thylakoid membranes in specific layers of the meristem 195

and in the leaf primordia. Developmental gradients can be observed from the base to the tip 196

(most matured chloroplasts), and from the margin to the midrib, within a given leaf in 197

Arabidopsis (Pogson et al., 2015; Gügel and Soll, 2016). However, the spatial (base-to-tip) 198

developmental gradient is more easily detected in monocotyledonous leaves (Pogson et al., 199

2015). 200

201

In angiosperms chloroplast biogenesis is dependent on light. Exposure to light leads to 202

extensive transcriptional reprograming, involving up to one third of the nuclear-encoded genes 203

that are either induced or repressed in response to light signals (Ma et al., 2001; Jiao et al., 204

2005; Dubreuil et al., 2017b). A significant number of the induced genes encode PhANGs. Light 205

and plastid signals regulate expression of the same group of photosynthesis-related genes and it 206

has been reported that light and retrograde signals are also mediated by cis elements found in 207

close proximity (Koussevitzky et al., 2007; Chi et al., 2013). Recent studies revealed that 208

nuclear genes encoding photosynthesis-associated genes, such as genes encoding light 209

harvesting antenna proteins and TBP enzymes, are enriched in G-box elements in their 210

promoters and could be regulated directly by HY5 and indirectly by GLKs, which are central 211

regulators of light and chloroplast development signalling, respectively (Lee et al., 2007; Waters 212

et al., 2009). This suggests a close interaction between these two signalling pathways that we 213

have recently begun to untangle. However, these two pathways can also act independently, as 214

retrograde signals from the plastid were also shown regulate PhANG expression in the dark 215

(Sullivan and Gray, 1999; Larkin, 2014). Interestingly, this specific feature of plastid signalling 216



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is observed in many gymnosperms where the seedlings green in the dark, and recent work from 217

pine suggested that activation of gymnosperm PhANGs in the dark may be regulated by a 218

plastid-to-nucleus signal (Hills et al., 2015). 219

220

The first regulatory step leading to the development of functional chloroplasts is the perception 221

of light by a set of photoreceptors, phytochromes (PHY) and cryptochromes (CRY), which 222

undergo conformational changes in order to interact with downstream proteins and initiate 223

intracellular signalling pathways (Jiao et al., 2007; Waters and Langdale, 2009). Genetic data 224

revealed that the blue light receptor CRY1 is involved in chloroplast development during blue 225

light induction and that the transcription factor HY5 is also involved in this pathway (Ruckle et 226

al., 2007) (Fig. 1). The red and far-red light receptors, the phytochromes, also regulate HY5 227

upon light activation but phytochrome signalling mainly proceeds through the Phytochrome-228

Interacting Proteins (PIFs), which are transcriptional repressors of chloroplast biogenesis (Jiao 229

et al., 2007). A recent quantitative mathematical model, validated in vivo, established a direct 230

link between light input via PHYB-PIF3 and the initiation of chloroplast development. The light 231

activated form of PHYB degrades PIF3, which represses the nuclear-encoded components of the 232

plastid transcriptional machinery required for transcription of the plastid-encoded 233

photosynthesis genes (Dubreuil et al., 2017a) (Fig. 1). pTAC12/HMR, one of the components 234

associated with the plastid-encoded RNA polymerase (PEP), was shown to be dually targeted to 235

the plastid and the nucleus. In the nucleus, pTAC12/HMR interacts with the photoactivated 236

PHYs, and PHY-pTAC12/HMR participates in the degradation of PIFs in the light, thereby 237

promoting photomorphogenesis (Chen et al., 2010; Galvão et al., 2012) (Fig. 1). The newly 238

synthetized pTAC12/HMR has a plastid transit peptide and is transported to the plastids where 239

it is processed for the subsequent nuclear localization. However, the mechanisms and regulation 240

of this translocation from the plastids to the nucleus is unknown (Nevarez et al., 2017). Detailed 241

investigations of the timing of pTAC12/HMR localisation during early light response and 242

chloroplast development could confirm the exciting proposition that pTAC12/HMR might be 243

involved in the co-ordination of photosynthetic gene expression in both the nucleus and the 244

chloroplast in response to light. 245

246

Two molecular pathways for the interaction of light and retrograde signals have recently been 247

described during the transition from skotomorphogenesis to photomorphogenesis in Arabidopsis 248

seedlings (Fig. 1). One of the pathways involves the GUN1-PTM-ABI4 retrograde signalling 249

module, which in this model antagonizes the COP1-HY5 light signal. During de-etiolation of 250

seedlings, ABI4 and HY5 integrate both signals by directly controlling the expression of a set of 251

genes involved in hypocotyl elongation and chloroplast development (Xu et al., 2016). 252

Moreover, the proposed pathway involves HY5 or ABI4 degradation by COP1. Conversely, 253



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HY5 and ABI4 both regulate the expression of COP1: ABI4 stimulates and HY5 inhibits 254

expression (Fig. 1). Thus, the balance between these three components provides the means to 255

fine-tune the response to light (Xu et al., 2016). 256

257

The second pathway describes the convergence of PHY-PIF-dependent light signal and the 258

GUN1-dependent retrograde signal. The interaction point is downstream of the PIFs and 259

antagonistically regulates the transcriptional photomorphogenic network (Martín et al., 2016). 260

This pathway is independent of ABI4; instead, the GUN1- and the PIF-dependent signals 261

converge on GLK1, repressing or inducing its expression, respectively. This transcriptional 262

control over GLK1 is both ABI4- and HY5-independent and the existing evidence suggests that 263

GLK1 is a direct target of PIF-mediated repression in the dark (Oh et al., 2012; Leivar and 264

Monte, 2014; Martín et al., 2016). In the model that has been proposed PIFs directly inhibit 265

GLK1 expression in the dark to support skotomorphogenesis. In the light, GLK1 expression is 266

released and allows photomorphogenesis to proceed. When the plastid is dysfunctional or 267

damaged, a GUN1-mediated retrograde signal represses GLK1 and attenuates 268

photomorphogenesis (Martín et al., 2016) (Fig. 1). 269

270

Clearly there is a close interaction between light and plastid signals but the timing of these two 271

signals during the normal progression of chloroplast biogenesis has been unclear. Early research 272

provided strong indications that a plastid retrograde signal is required for full expression of the 273

nuclear-encoded photosynthetic genes (Sullivan and Gray, 1999). Blocking PEP-driven plastid 274

transcription with rifampicin or using mutants of various PEP components blocked PhANG 275

expression in a light-independent way (Woodson et al., 2013). However, a recent comparative 276

transcriptomic analysis of seedlings grown in light or dark, and the albino pap7 mutant, 277

revealed that altered PGE and blocked plastid development does not affect global PhANG 278

expression (Grübler et al., 2017). On the other hand, a new model where the light response has 279

been investigated in an Arabidopsis cell culture with very high temporal resolution of the 280

chloroplast developmental process, suggests that the light signal precedes a plastid signal 281

(Dubreuil et al., 2017b). Two phases were clearly observed in the expression profile of the 282

PhANGs in the cell culture. The first phase is dependent on light and triggers changes that will 283

initiate chloroplast development, and more importantly initiates expression of the PEP 284

components. The second phase is dependent on the activation of the chloroplast as the second 285

phase of PhANG induction was absent when chloroplast development was blocked (Dubreuil et 286

al., 2017b). 287

288

The nature of the plastid signal, whether is it a negative or a positive signal, is another open 289

question and different hypotheses have been proposed over the years (Pfannschmidt, 2010; 290



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Terry and Smith, 2013). However, recent experimental work goes some way to clarifying this 291

question. Supporting the early study by Sullivan and Gray (Sullivan and Gray, 1999) the work 292

of Martín et al. (2016) demonstrated that the inhibitory effect of lincomycin blocks the 293

photomorphogenic responses early and rapidly, indicating that the retrograde signal is already 294

present in the proplastids/etioplasts, or is developed rapidly in response to defective chloroplasts 295

in order to prevent normal development in light. The results from the experiments by Martín et 296

al. (2016) can be interpreted in two ways: (1) a positive signal from intact plastids that is 297

necessary for GLK1 expression is interrupted by plastid dysfunction in a GUN1-dependent 298

manner, or (2) functional chloroplasts do not emit signals, whereas dysfunctional chloroplasts 299

generate a GUN1-dependent negative signal that represses GLK1 expression. Support for the 300

positive nature of the plastid signal comes from analyses of LHCB expression in pine, where 301

LHCBs are expressed in the dark and thus PhANG expression was shown to be independent of 302

light but dependent on plastid-to-nucleus signals (Hills et al., 2015). These authors proposed an 303

evolutionary model in which angiosperms recruited light signalling repressors to supress the 304

response of PhANGs to a positive plastid signal present also in the dark (Hills et al., 2015). 305

Furthermore, modelling of expression data from the plastid and the nuclear genomes strongly 306

suggests that the plastid signal required for full PhANG induction is positive in nature (Dubreuil 307

et al., 2017b). In addition, it was recently shown using the prin2 mutant that LHCB expression 308

was directly correlated with the recovery of PEP activity in the prin2 mutant complemented 309

with differet PRIN2 variants. It was further suggested that a positive signal is generated by PEP 310

activity in the plastids that stimulates LHCB expression in the nucleus (Diaz et al., in press). On 311

the other hand, the transcriptomic results using pap7 seedlings have identified different sets of 312

genes regulated either by healthy chloroplast or arrested plastids, respectively, suggesting the 313

existence of both positive and negative signals (Grübler et al., 2017). 314

315

5. HIGHER ORDER RESPONSES IN THE NUCLEUS TO RETROGRADE SIGNALS 316

Light has been shown to induce changes in splicing activity (Petrillo et al., 2014; Shikata et al., 317

2014; Hernando et al., 2017) and the splicing pattern of specific splicing factors involved in 318

dark-to-light shifts is regulated in response to the redox status of PET. Proper splicing of these 319

factors was proposed to play a role in the adaptation of the photosynthetic machinery to changes 320

in the light conditions (Petrillo et al., 2014). However, more experimental work is required to 321

identify the components that regulate splicing in response to retrograde signals, the genes 322

affected, and how those changes affect plant development and photosynthetic activity. 323

324

Light has been shown to induce changes to nuclear size and architecture that correlate with 325

transcriptional changes (Bourbousse et al., 2015; Perrella and Kaiserli, 2016). A specific light-326

regulated loci, CAB, was shown to relocate to the nuclear periphery just before transcriptional 327



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induction in a PHYA, PHYB, PIFs, COP1 and DET1-dependent manner (Feng et al., 2014). A 328

change to the nuclear position was also observed for the photosynthesis-related genes RBCS1A, 329

GUN5, and PC, supporting the model of repositioning of loci to the nuclear periphery as a 330

mechanism to activate gene expression in response to light (Feng et al., 2014). So far, neither 331

the repositioning of the gene loci nor the changes to nuclear architecture have been linked to 332

retrograde signals but due to the close relationship between light and plastid signals, a detailed 333

analysis of a potential contribution of plastid signals to those interesting features would be 334

worth pursuing. 335

336

In addition, the proportion of heterochromatin was shown to change in light exposed cotyledons 337

in a CRY1/CRY2-DET1/COP1-HY5 dependent manner (Bourbousse et al., 2015) and RNA-338

seq, in combination with DNase I hypersensitive site sequencing, revealed that the level of 339

chromatin condensation in darkness is correlated with blocked expression of light and 340

photosynthesis related genes. The genes affected by changes in chromatin condensation are 341

enriched in plastid signalling-related genes and their promoters frequently contain the GLK1 342

binding elements (Liu et al., 2017), but at this point no clear link between retrograde signal(s) 343

and chromatin changes has been established. Currently much research attention is directed 344

towards the connection between metabolism and chromatin dynamics in animal systems. Thus, 345

exploring the dynamics of global chromatin organization during chloroplast development is a 346

critical future direction for plant sciences. 347

348

349

6. THE IMPACT OF RETROGRADE SIGNALS ON WHOLE PLANT PHYSIOLOGY 350

AND DEVELOPMENT 351

Chloroplast function and integrity are important not only for seedling development during the 352

transition to photomorphogenesis but also for leaf and plant development throughout the entire 353

plant life cycle. The importance of chloroplast activity during seed and embryo development is 354

reflected in the large number of essential proteins localized to the chloroplast, many of them 355

involved in plastid gene expression. The complete loss of SIG5 or RUG2/BSM results in 356

embryo-lethal phenotypes (Hsu et al., 2010; Babiychuk et al., 2011; seedgene.org). The 357

significant role of PEP activity and therefore PGE-triggered retrograde signalling during 358

embryo development was further supported by the embryo pigment defective phenotype of 359

mutants in PEP components, like pTAC3 or MurE, or with altered PEP activity, like PRIN2 360

(Garcia et al., 2008; Kremnev and Strand, 2014; seedgene.org). Similarly, the complete loss of 361

essential components of the plastid ribosomal complex, like ClpP proteins or Plastid Ribosomal 362

Protein S5 (PRPS5, Scabra1), also results in embryo-lethality (Pogson and Albrecht, 2011; 363

Mateo-Bonmatí et al., 2015). Furthermore, the NEP-defective sca3 mutant demonstrated 364



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reticulate patterns with perturbed mesophyll cell differentiation (Hricová et al., 2006). In 365

addition, several anu (angulata) mutants with abnormal leaf development are affected in genes 366

encoding chloroplast proteins (Casanova-Saez et al, 2014, Muñoz-Nortes et al, 2017). ANU7 is 367

involved in the regulation of PGE and PhANG expression and interacts genetically with GUN1, 368

indicating a role for retrograde signals in the development of leaf lamina and mesophyll cells 369

(Muñoz-Nortes et al, 2017). PGE was specifically shown to regulate leaf abaxial-adaxial pattern 370

in a GUN1-dependent manner, affecting the expression of specific genes that control 371

asymmetric abaxial-adaxial differentiation (Tameshige et al., 2013). Thus, mutants with 372

impaired plastid development have revealed the close relationship between plastid integrity and 373

leaf development (Aluru et al., 2006; Casanova-Sáez et al., 2014; Lundquist et al., 2014; Van 374

Dingenen et al., 2016; Muñoz-Nortes et al., 2017). 375

376

The classic variegated Arabidopsis mutant immutans, is defective in PTOX and the hypothesis 377

for the formation of the white and green sectors is based on a threshold model where the 378

variegation is dependent on the redox and excitation pressures during the early stages of 379

chloroplast biogenesis when the thylakoid membranes are being formed. The green sectors in 380

the im mutants emerge from plastids that managed to escape the over-reduction of the 381

membrane by the action of compensating factors that affect the excitation pressure threshold 382

(Kambakam et al., 2016; Pogorelko et al., 2016). Using detailed kinematic and gene expression 383

studies, it was shown that the leaf becomes photosynthetically active at the same time as it shifts 384

from primary to secondary morphogenesis (Andriankaja et al., 2012). Thus, chloroplast 385

differentiation is an important regulator of the simultaneous onset of cell expansion and 386

photosynthesis. Furthermore, it was suggested that retrograde signalling through tetrapyrroles 387

plays a role in the shift to cell expansion and activation of photosynthesis (Andriankaja et al., 388

2012). 389

390

Regulation of flowering time in response to plastid signals was indicated by the flowering 391

phenotypes of mutants like crd (which over-accumulates MgProto-IX and MgProto-IX-ME), 392

mutants with impaired NEP activity, and the sco1 mutant that is defective in the plastid 393

elongation factor G (Baba et al., 2004; Albrecht et al., 2006; Barajas-López et al., 2013). A 394

model has been proposed where chloroplasts act as stress sensors that transmit information to 395

the nucleus to regulate flowering-related gene expression and thereby also the timing of the 396

plant life cycle. MEcPP, a plastid metabolite that plays a role in a stress induced retrograde 397

signalling pathway, also regulates flowering time through the regulation of the transcription 398

factor BBX19, which interacts with CO to regulate FT expression (Wang et al., 2014). In 399

addition, the cleaved N-PTM transcription factor was shown to be involved in the repression of 400



12

the flowering time regulator FLC by recruiting FVE and interacting with the promoter of FLC 401

(Feng et al., 2016). 402

403

The GLK transcription factors have been shown to be implicated in fruit development, for 404

example through the pale siliques of the Arabidopsis glk2 mutant or the identification of GLK2 405

as the locus affected in the uniform ripening (u) mutation that results in uniformly green 406

tomatoes (Waters et al., 2008; Powell et al., 2012; Nguyen et al., 2014). Similarly, a correlation 407

was reported between CaGLK2 and variation in chlorophyll content and colour in pepper fruit 408

(Brand et al., 2014). However, a clear involvement of a retrograde signal controlling GLK2 409

expression and/or activity during fruit development remains to be demonstrated. A theoretical 410

model referred to as “degradational control” has been proposed where the degradation of 411

Rubisco during senescence, as a source of nitrogen, and its export out of the chloroplast 412

constitute a potential retrograde signal (Pfannschmidt, 2010). Senescence is a highly-controlled 413

light- and/or age-dependent program that is accompanied by a transcriptional reprograming. The 414

light-dependent signalling pathway (PHYB-PIFs-GLKs) involved in senescence is equivalent to 415

the light-signalling pathway regulating chloroplast biogenesis, but the outcome is repression 416

rather than induction of the GLKs and PhANGs (Liebsch and Keech, 2016). However, as is the 417

case for fruit development, the involvement and nature of a plastid retrograde signal in the 418

senescence process has yet to be experimentally demonstrated. 419

420

7. CONCLUDING REMARKS 421

The field of plastid-to-nucleus signaling has been very dynamic over the last few years and 422

there have been several major breakthroughs leading to a much more advanced understanding of 423

the mechanisms involved in the communication between the plastids and the nucleus. These 424

recent findings, as highlighted in this review, have made it clear that chloroplast development is 425

controlled by a delicate interplay between light and plastid signalling pathways. In addition, a 426

number of key players involved in this interplay are now identified (Advances box). Critical 427

future directions for this field of plant sciences include efforts to finally understand the 428

mechanism of the elusive key signaling component GUN1, to identify cytosolic components 429

acting as signal transducers from the chloroplast to the nucleus, and to explore the dynamics of 430

global chromatin organization in response to retrograde signals and the establishment of 431

photosynthesis (Outstanding questions box). 432

433

434

8. ACKNOWLEDGEMENTS 435



13

We apologize to the authors who did not get their work discussed in this review due to space 436

limitations. Funding from the Swedish Research Council (VR) is acknowledged. 437

438

439

440

441

442



14

443 Figure 1. Model of retrograde signalling during chloroplast biogenesis. Chloroplasts 444

develop from etioplast or proplastids in response to light. In the dark, and in the 445

etioplasts/proplastids the plastid encoded genes are mainly transcribed by NEP, and PET and 446

TBP are not functional (dashed line boxes). During the greening process, activation of PEP 447

plays a major role. PEP activity requires the rpo core components, SIGMA factors (SIG), PEP-448

associated proteins (PAPs, like pTAC12), and other proteins located in the nucleoid, like 449

PRIN2. PRIN2 is involved in the light regulation of PEP activity. The disruption of PET, TBP, 450

or PGE, generates a signal that is transduced by GUN1. It is to date unknown if the retrograde 451

signal is of a positive nature that is interrupted in case of chloroplast disruption (for example by 452

GUN1), or if the disrupted chloroplasts emit a negative signal (that can be mediated by GUN1). 453

In response to chloroplast signals, PTM is cleaved, and the N-PTM form is translocated to the 454

nucleus where it activates ABI4 expression, inhibiting LHCBs expression and promoting the 455

expression of COP1 and genes involved in hypocotyl elongation. In the dark, HY5 is degraded 456

by COP1, that also degrades ABI4. The PIFs repress a set of PhANGs, the GLKs and genes 457

encoding the nuclear encoded PEP components. In the light, the light perception by the 458

photoreceptors, CRY1 and PHYs, causes exclusion of COP1 from the nucleus and degradation 459

of the PIFs. The chloroplast-localized pTAC12 is an essential part of the PEP complex, but is 460

also processed and translocated to the nucleus. The nuclear pTAC12 interacts with the active 461

form of PHYs (Pfr) and contributes to PIF degradation. The exclusion of COP1 allows for 462

accumulation of HY5. Degradation of PIFs releases the transcription of the GLKs and other set 463

of genes like the genes encoding the PEP component. HY5 and GLKs induce PhANGs (LHCBs 464

and genes coding TBP enzymes, among others) expression, represses COP1 and the elongation-465

related genes. (Figure by Daria Chrobok). 466

467

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22

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706

707



PhANGs

COP1 TBPLHCBs

TBP

rpoPGE

CRY1

PTM

PGE

PTM

Pfr

PIFs

Blue Light

CRY1

Light PHYs

PrPHYs

GUN1GUN1

Pfr

COP1 ELONGATION ELONGATIONLHCBs

N-PTM

TF

TFPIFs

PIFs

PIFs

TBP

ABI4 GLKsHY5

ABI4

GLKs

PEP components

ABI4

GLKs

PEP components

NEPhousekeeping

genes

PET

PRIN2

pTAC12

rpoSIGPAPs photosynthesis

genes

nucleus nucleus

etioplast/proplastidchloroplast

?

NEPplastid genes

TBP

PET

pTAC12

pTAC12

Dark Light

pTAC12

HY5

COP1

COP1

COP1

positive regulation

negative regulation

protein degradation

established pathways

putative pathways



ADVANCES

• Chloroplast function and integrity impacts leaf and plant development throughout the entire plant life cycle.

• During leaf development, chloroplast differentiation is an important regulator of the simultaneous onset of cell expansion and photosynthesis.

• The light induction of PhANGs during chloroplast development occurs in two essential regulatory phases: a photoreceptor-mediated phase and a phase controlled by a plastid signal, where the light signal precedes the plastid signal.

• Two mechanistic modules have been shown to control chloroplast development: the convergence of the PHY-PIFs-dependent light signal and the GUN1-dependent retrograde signal, and the GUN1-PTM-ABI4 retrograde signaling module which antagonize the COP1-HY5 light signal.



OUTSTANDING QUESTIONS

• What is the nature of the retrograde signal(s) during seedling establishment? Is it a positive signal from functional chloroplasts or a negative signal from disrupted chloroplasts, or both?

• What is the molecular mechanism behind the function of the key player GUN1 and what is the timing of GUN1 action?

• Which are the cytosolic transducers of plastid signals to the nucleus?

• What is the impact of retrograde signals on chromatin modifications and nuclear architecture?



BOX 1. The genomes uncoupled Mutants

The Arabidopsis genomes uncoupled mutants were identified in a forward genetic screen using the herbicide Norflurazon that inhibits carotenoid biosynthesis and thereby blocks chloroplast biogenesis. The expression of two transgenes under the control of the chlorophyll a/b-binding protein3 (CAB3) promoter was used to screen the mutagenized population for transcription of CAB3 that was uncoupled from the functional state of the chloroplast (Susek et al., 1993). The screen resulted in the isolation of several gun mutants, all of them with mutations in genes encoding chloroplasts-localized proteins:

• gun1 is defective in a pentatricopeptide-repeat protein that integrates TBP-, PGE-, and PET-derived signals. Additional gun1 alleles have been isolated in different screens using the Luciferase reporter gene under the control of CAB promoter. Of the gun mutants, gun1 is the only mutant that shows

• the gun phenotype when grown with Lincomycin, and also in response to high light, clearly indicating a role of GUN1 in the response to disturbed PGE and PET (Koussevitzky et al., 2007).

• gun2 and gun3 are defective in heme oxygenase and phytochromobilin synthase, respectively,

enzymes that convert Heme to Phytochromobilin. The gun2 and gun3 accumulate more Heme but less chlorophyll compared to wild type. The pale phenotypes were explained by a negative regulation of Heme on TBP (Mochizuki et al., 2001).

• gun4 and gun5 are defective in a novel Mg-ProtoIX-binding protein and in the H-subunit of Mg-chelatase, respectively. Mg-chelatase is the first specific TBP enzyme of chlorophyll biosynthesis, and both gun4 and gun5 accumulate lower levels of chlorophyll compared to wild type (Mochizuki et al., 2001).

In an alternative screen using activation-tagged mutagenesis, an additional gun mutant was identified, gun6:

• gun6-1D is a dominant gain-of-function mutant of Ferrochelatase 1 (FC1), the enzyme upstream of GUN2 and GUN3 in the biosynthesis pathway of Heme (Woodson et al., 2011).



BOX 2. The Plastid Transcription Complexes, NEP and PEP. Chloroplast genes are transcribed by two types of RNA polymerases; the nuclear-encoded plastid RNA polymerase (NEP) and the plastid-encoded RNA polymerase (PEP). Essential for proper chloroplast development is a shift in the usage of the major RNA polymerase from NEP to PEP. NEP is a nuclear-encoded phage-type single subunit polymerase that is encoded by the RNA polymerase of the phage T3/T7 type (RPOT) genes, while PEP is a multisubunit RNA polymerase inherited from the cyanobacterial ancestor. The PEP core subunits are encoded by the rpo plastid genes, but PEP requires the nuclear-encoded sigma factors for promoter recognition and a large number of other proteins referred to as PEP-associated proteins (PAPs) or Transcriptionally Active Chromosome proteins (pTACs), for its function. Several mutants have been reported in NEP, PEP, or PEP-associated proteins and those mutations trigger the PGE retrograde signal:

• scabra3 (sca3) is defective in the exclusively plastid-localized RPOTp of NEP. SCA3 is essential for chloroplast biogenesis, and the mutants have pale or yellowish cotyledons and leaves (Hricová et al., 2006).

• sigma2 and sigma6 (sig2 and sig6) are defective in the SIGMA2 and -6 proteins that are essential for

the DNA sequence recognition of PEP during chloroplasts development and the mutant seedlings are pale (Woodson et al., 2013).

• ptac12/hemera is defective in the dual-localized protein pTAC12/HMR that is associated with PEP. The protein is essential for PEP activity and chloroplast development in the light, which is reflected in the albino phenotype of the mutant. In addition to the role of pTAC12/HMR in the plastids, the protein could potentially act as a plastid signal transducer as it has also been identified in the nucleus associated with Phy (Chen et al., 2010; Galvão et al., 2012; Nevarez et al., 2017).

• pap7/ptac14 is defective in PAP7 protein that is associated with PEP. pap7 mutant seedlings are albino and defective in PEP-dependent transcription (Gao et al., 2011)

• prin2 is defective in Plastid Redox Insensitive2 (PRIN2), a novel protein that interacts with TRXz and is essential for light induced activation of PEP. prin2 mutants are pale and have impaired chloroplasts (Kindgren et al., 2012; Kremnev and Strand, 2014; Díaz et al., 2017).



Parsed CitationsAlbrecht V, Ingenfeld A, Apel K (2006) Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact ofchloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol Biol 60: 507–518

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Aluru MR, Yu F, Fu A, Rodermel S (2006) Arabidopsis variegation mutants: new insights into chloroplast biogenesis. J Exp Bot 57:1871–1881


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Avendaño-Vázquez A-O, Cordoba E, Llamas E, San Román C, Nisar N, De la Torre S, Ramos-Vega M, Gutiérrez-Nava M d. l. L,Cazzonelli CI, Pogson BJ, et al (2014) An uncharacterized apocarotenoid-derived signal generated in carotene desaturase mutantsregulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 26: 2524–2537


Baba K, Schmidt J, Espinosa-Ruiz A, Villarejo A, Shiina T, Gardeström P, Sane AP, Bhalerao RP (2004) Organellar gene transcriptionand early seedling development are affected in the rpoT;2 mutant of Arabidopsis. Plant J 38: 38–48


Babiychuk E, Vandepoele K, Wissing J, Garcia-Diaz M, De Rycke R, Akbari H, Joubès J, Beeckman T, Jänsch L, Frentzen M, et al (2011)Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family.Proc Natl Acad Sci U S A 108: 6674–6679


Barajas-López J de D, Kremnev D, Shaikhali J, Piñas-Fernández A, Strand Å (2013) PAPP5 is involved in the tetrapyrrole mediatedplastid signalling during chloroplast development. PLoS One 8: e60305


Bobik K, Burch-Smith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6: 781Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bourbousse C, Mestiri I, Zabulon G, Bourge M, Formiggini F, Koini MA, Brown SC, Fransz P, Bowler C, Barneche F (2015) Lightsignaling controls nuclear architecture reorganization during seedling establishment. Proc Natl Acad Sci U S A 112: E2836-2844


Bradbeer JW, Atkinson YE, Börner T, Hagemann R (1979) Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesised RNA. Nature 279: 816–817


Brand A, Borovsky Y, Hill T, Rahman KAA, Bellalou A, Van Deynze A, Paran I (2014) CaGLK2 regulates natural variation of chlorophyllcontent and fruit color in pepper fruit. Theor Appl Genet 127: 2139–2148


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http://www.ncbi.nlm.nih.gov/pubmed?term=Gao Z%2DP%2C Yu Q%2DB%2C Zhao T%2DT%2C Ma Q%2C Chen G%2DX%2C Yang Z%2DN %282011%29 A functional component of the transcriptionally active chromosome complex%2C Arabidopsis pTAC14%2C interacts with pTAC12%2FHEMERA and regulates plastid gene expression%2E Plant Physiol 157%3A 1733�??45Garcia M%2C Myouga F%2C Takechi K%2C Sato H%2C Nabeshima K%2C Nagata N%2C Takio S%2C Shinozaki K%2C Takano H %282008%29 An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development%2E Plant J 53%3A 924�??934&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kremnev D%2C Strand � %282014%29 Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis%2E Front Plant Sci 5%3A 385&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Larkin RM %282014%29 Influence of plastids on light signalling and development%2E Philos Tansactions R Soc 369%3A 20130232&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nevarez P%2C Qiu Y%2C Inoue H%2C Yoo CY%2C Benfey PN%2C Schnell DJ%2C Chen M %282017%29 Mechanism of dual targeting of the phytochrome signaling component HEMERA%2FpTAC12 to plastids and the nucleus%2E Plant Physiol 173%3A 1953�??1966&dopt=abstract

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retrograde signals navigate the path to chloroplast …...mutations in sig2, sig6 and prin2...

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