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1 Update on Photomorphogenesis 1 Seedling establishment: a dimmer switch-regulated process between dark 2 and light signaling 3 4 Charlotte M. M. Gommers and Elena Monte* 5 6 *Author for correspondence 7 8 Affiliation: 9 Plant Development and Signal Transduction Program, Center for Research in Agricultural 10 Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra, Barcelona, Spain. 11 12 Short title: Dark and light signals shape seedling establishment 13 14 Corresponding author: Elena Monte, [email protected] 15 16 Author contributions: C.M.M.G and E.M. wrote the manuscript, C.M.M.G. composed the 17 figures. 18 19 Single sentence summary: A balance between dark and light signaling directs seedling 20 establishment through integrating internal and environmental information. 21 22 The authors declare no conflict of interest. 23 24 Funding information: The laboratory is supported by grants from the Spanish “Ministerio de 25 Economía y Competitividad” (MINECO) BIO2015-68460-P, and from the Generalitat de 26 Catalunya 2014-SGR-1406 to E.M. We acknowledge financial support by the CERCA 27 programme/Generalitat de Catalunya and from MINECO through the “Severo Ochoa 28 Programme for Centers of Excellence in R&D” 2016-2019 (SEV20150533)”. 29 30 Corresponding author e-mail: [email protected] 31 32 33 Plant Physiology Preview. Published on December 7, 2017, as DOI:10.1104/pp.17.01460 Copyright 2017 by the American Society of Plant Biologists www.plantphysiol.org on October 15, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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Page 1: Update on Photomorphogenesis - Plant Physiology...2017/12/07  · 1406 to E.M. We acknowledge financ ial support by the CERCA 28 programme/Generalitat de Catalunya and from MINECO

1

Update on Photomorphogenesis 1

Seedling establishment: a dimmer switch-regulated process between dark 2

and light signaling 3

4

Charlotte M. M. Gommers and Elena Monte* 5

6

*Author for correspondence 7

8

Affiliation: 9

Plant Development and Signal Transduction Program, Center for Research in Agricultural 10

Genomics (CRAG), CSIC-IRTA-UAB-UB, Campus UAB, Bellaterra, Barcelona, Spain. 11

12

Short title: Dark and light signals shape seedling establishment 13

14

Corresponding author: Elena Monte, [email protected] 15

16

Author contributions: C.M.M.G and E.M. wrote the manuscript, C.M.M.G. composed the 17

figures. 18

19

Single sentence summary: A balance between dark and light signaling directs seedling 20

establishment through integrating internal and environmental information. 21

22

The authors declare no conflict of interest. 23

24

Funding information: The laboratory is supported by grants from the Spanish “Ministerio de 25

Economía y Competitividad” (MINECO) BIO2015-68460-P, and from the Generalitat de 26

Catalunya 2014-SGR-1406 to E.M. We acknowledge financial support by the CERCA 27

programme/Generalitat de Catalunya and from MINECO through the “Severo Ochoa 28

Programme for Centers of Excellence in R&D” 2016-2019 (SEV‐ 2015‐ 0533)”. 29

30

Corresponding author e-mail: [email protected] 31

32

33

Plant Physiology Preview. Published on December 7, 2017, as DOI:10.1104/pp.17.01460

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon October 15, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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Abstract 34

By being exquisitely sensitive to their light surroundings, plants are able to continuously 35

adjust their growth to optimize fitness. Darkness is an important cue for plants and a time 36

when they actively grow and develop through regulation of the appropriate gene networks 37

and biochemical changes. Although plants might not posses “dark receptors”, inactive 38

photoreceptors facilitate activation and inhibition of dark-specific processes, and thus 39

darkness itself might be considered a signal triggering a myriad of responses. In this Update, 40

we review the effects of dark and light signaling during seedling establishment. We describe 41

the features of seedlings germinated in the dark and their switch in development upon 42

emerging into the light. We examine how aboveground growth is regulated by the duration of 43

dark/light cycles, and how circadian clock signaling is integrated. Finally, we discuss some of 44

the challenges faced by young seedlings during their establishment, such as variations in 45

temperature or in light quality and quantity. Although briefly mentioned, we do not cover in 46

detail the contribution of sugars or temperature to seedling establishment in response to dark 47

and light signals; we refer readers to excellent recent reviews (Franklin et al., 2014; Legris et 48

al., 2017; Seluzicki et al., 2017). The emerging view is that of seedling establishment 49

regulated as a dimmer-type switch where relative amounts of dark and light signaling 50

dynamically optimize plant development to the surrounding light environment. 51

52

53

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Seedling establishment is first heterotrophic and fueled by seed reserves 54

The process of seedling establishment starts with seed germination, when the newly emerging 55

seedling grows heterotrophically on seed reserves, and it is completed when the seedling has 56

gained photosynthetic competence and becomes autotrophic. It is one of the most critical and 57

vulnerable processes in the life of a plant, and it often represents a challenge after emerging 58

from the protected environment of the seed. Until the seedling reaches photoautotrophy, post-59

germinative seedling development is fueled on seed storage reserves. These nutrient reserves 60

are deposited in the seed during seed maturation in the mother plant, and consist of oil, 61

storage protein and/or carbohydrates (usually starch), depending on the plant species. 62

Reserves can remain intact as insoluble compounds in desiccated seeds for extended periods 63

of time. The predominant storage tissue in some plant species such as the oilseed castor bean 64

is the endosperm, whereas in others, with a greatly reduced endosperm, is the embryo 65

(Eastmond and Graham, 2001). Upon seed germination, reserves are mobilized into soluble 66

metabolites to fuel growth and achieve establishment before seed nutrients are depleted. The 67

efficiency of reserve mobilization is associated with seedling vigor, a key determinant of 68

seedling establishment and crop yield in the field (Finch-Savage and Bassel, 2017). 69

Lipid in the form of triacylglycerol (TAG) is the main seed reserve in many plant 70

species such as Arabidopsis thaliana or the oilcrops soybean, sunflower, rapeseed, safflower, 71

and maize (Graham, 2008). In Arabidopsis, about 90% of the reserves (TAGs and protein) 72

are stored in the cotyledons, and the rest in the endosperm (Penfield et al., 2004). Through 73

gluconeogenesis, plants make sugars from lipid and protein stores to fuel seedling 74

establishment. In fact, Arabidopsis lipid reserve mobilization is critical for seedling 75

establishment (Kelly et al., 2011). Whereas oils in the cotyledons fuel their transformation 76

into photosynthetic organs, oils in the endosperm fuel hypocotyl growth in the dark. In 77

several plant species such as Arabidopsis, rapeseed (Brassica napus), cucumber (Cucumis 78

sativus), and sunflower (Helianthus annuus), lipid reserve mobilization is enhanced by light 79

(Theimer and Rosnitschek, 1978; Davies et al., 1981; Sadeghipour and Bhatla, 2003; Leivar 80

et al., 2009). In others species like mustard (Sinapis alba) or tomato (Solanum lycopersicum), 81

light appears not to regulate oil mobilization but the activity of two key enzymes of the 82

glyoxylate cycle (isocitrate lyase and malate synthase) involved in the synthesis of glucose 83

from the acetate generated in fatty acid β-oxidation (Bajracharya and Schopfer, 1979; 84

Eckstein et al., 2016). The lipases sugar dependent 1 (SDP1) and SDP1-like (SDP1L) 85

account for 95% of post-germinative TAG degradation in Arabidopsis, given that a double 86

mutant sdp1sdp1l is unable to breakdown any storage oil (Eastmond, 2006; Kelly et al., 87

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2011). However, it is still not clear whether the light enhanced oil mobilization during 88

seedling establishment involves increased levels or activity of these lipases. 89

90

Out of dark and into the light: Switching the balance from dark- to light signaling 91

induces autotrophic photomorphogenesis 92

When buried under the soil, directly after germination, a seedling’s mission is to grow 93

towards the light as soon as possible. This is facilitated by rapid elongation of the embryonic 94

stem, the hypocotyl, accompanied by a hook in its most apical part to protect the shoot apical 95

meristem. During this so-called skotomorphogenic growth, cotyledons and roots remain 96

underdeveloped. Reaching the soil surface and the light, the young seedling has to establish a 97

photoautotrophic lifestyle. The light is perceived by several classes of photoreceptors, which 98

induce a signaling cascade towards photomorphogenic development (Box 1) that lead to 99

extreme, organ-specific, developmental changes that require local promotion (cotyledons, 100

roots) and inhibition (hypocotyl) of growth (Fig. 1). Seedling photomorphogenesis is mostly 101

studied in the model species Arabidopsis, but is common among a wide variety of plant 102

species. In the field, successful crop seedling establishment is essential for plant growth and 103

yield (Finch-Savage and Bassel, 2017). Most diploid species experience photomorphogenic 104

changes similar to Arabidopsis (see the examples of tomato and quinoa in Fig. 2), while dark-105

grown monocots typically elongate the coleoptile to protect the first true leaf in the dark and 106

then stop elongation upon exposure to light (example of sorghum in Fig. 2). In the next 107

section, we highlight the plant organs that undergo the most striking developmental switch 108

when an Arabidopsis seedling grows out of the dark and into the light: the apical hook, the 109

cotyledons, the hypocotyl, and the root. 110

111

The apical hook 112

Soon after germination, darkness triggers asymmetrical cell expansion and division at the 113

apical part of the hypocotyl, which results in bending. Expansion of the inner (concave) cells 114

is inhibited, while division in the outer (convex) cells is promoted (Silk and Erickson, 1978; 115

Raz and Koornneef, 2001), which forms an apical ‘hook’, bending up to 180 degrees (Fig. 116

3A). This asymmetrical cell expansion is caused by an auxin maximum in the concave part of 117

the hook, created by auxin in- and out flux carriers (AUXIN1 (AUX1) and LIKE-AUX1 118

(LAX)), and (PIN-LIKE (PIN) proteins, respectively) in the epidermal cells of the young 119

hypocotyl (Box 1; Žádníková et al., 2010; Žádníková et al., 2016; Farquharson, 2017). In 120

darkness, PHYTOCHROME INTERACTING FACTORS (PIFs; Box 1; reviewed in this 121

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focus issue by Pham et al., 2017) enhance auxin synthesis and signaling, and the synthesis of 122

two other important hormones in hook formation and maintenance: ethylene (ET) and 123

gibberellic acid (GA) (Box 2; reviewed by Mazzella et al., 2014). Ethylene signaling via 124

transcription factors ETHYLENE INSENSITIVE3 (EIN3) and EIN3-LIKE1 (EIL1) induces 125

local PIN gene expression in the epidermis and auxin transport (Žádníková et al., 2016). 126

Accordingly, exogenous treatment with ethylene causes exaggerated hooks in Arabidopsis 127

(Gallego-Bartolomé et al., 2011). GA appears essential for hook formation as the inhibitor of 128

DELLA proteins, which, in the absence of GA, inhibit both PIFs and EIN3/EIL1 (Box 2; 129

(Feng et al., 2008; de Lucas et al., 2008; Gallego-Bartolomé et al., 2011; An et al., 2012). As 130

a consequence, the constitutive DELLA-expressing mutant gai-1 is unable to form a hook in 131

the dark, and della loss-of-function mutants have exaggerated hooks (Gallego-Bartolomé et 132

al., 2011). Although continuous dark periods will slowly cause opening of the apical hook 133

(Raz and Ecker, 1999), this process is significantly enhanced by a light signal (Fig. 1). Light 134

activates phytochromes (phys) and cryptochromes (CRYs), which directly target and degrade 135

PIFs, as well as EIN3 (Box 1; Shi et al., 2016b). This causes a rapid loss of GA, ET signaling 136

and the directional auxin gradient, which enhances cell expansion in the concave part of the 137

hook, followed by opening (Fig. 3A). 138

139

The cotyledons 140

While in the dark, cotyledons have little to no function and remain closed. Once in the light, 141

cotyledons have to undergo important developmental changes to allow for efficient 142

photosynthesis to fuel autotrophic growth (Fig. 3B): 143

Separation and expansion. Dark grown seedlings have relatively small epidermal 144

pavement cells, which results in small cotyledon areas (Wei et al., 1994). HY5-mediated 145

cotyledon cell division and expansion is suppressed in darkness by PIFs and COP1 146

(Stoynova-Bakalova et al., 2004; Xu et al., 2014). Light releases the suppression of HY5 147

(Box 1) and thus allows cotyledon expansion (Josse et al., 2011). 148

Stomata development. Light induces stomata development to allow for gas exchange 149

between the plant and the environment. Stomata are epidermal pores, formed by two guard 150

cells with thick elastic walls that resist the high turgor pressure generated during opening. In 151

Arabidopsis, stomatal development is characterized by a series of epidermal cell divisions. In 152

the cotyledons, a subset of protodermal cells can become a meristemoid mother cell (MMC) 153

committed to the stomatal pathway. The MMC divides asymmetrically to give rise to a small 154

meristemoid (M) and a large sister cell. The M can undergo two further asymmetrical 155

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divisions to increase the number of the total epidermal cells or differentiate into a guard 156

mother cell (GMC). The GMC then gives rise to two guard cells (GC) that form the stoma. 157

The larger sister cell can become a pavement cell or undergo additional asymmetric spacing 158

divisions to generate satellite Ms away from the existing stoma (the “one-cell spacing rule”) 159

(Pillitteri and Torii, 2012; Wengier and Bergmann, 2012). Regardless of light conditions, Ms 160

are generated during the first two days of seedling establishment. In darkness, their 161

development is then arrested (Wei et al., 1994), by the active COP1-SPA complex (Kang et 162

al., 2009). GC differentiation is completed in both the hypocotyl and the expanding 163

cotyledons (Wei et al., 1994), mediated by CRYs, phyA, and phyB, with phyB having a 164

dominant role in white light. The COP1-SPA interaction is inhibited (Box 1), and PIF4 fine-165

tunes stomatal development in response to light quantity (Casson et al., 2009). The 166

consecutive steps in stomata differentiation are regulated by three bHLH transcription factors 167

(MUTE, SPEECHLESS (SPCH) and FAMA) downstream of a MAP kinase signaling 168

cascade regulated by light quantity (reviewed in Lau and Bergmann, 2012). 169

Chloroplast development and pigment biosynthesis. In higher plants, all cells contain 170

plastids derived from embryonic proplastids. In darkness, seedling proplastids develop into 171

etioplasts, which contain a prolamellar body that incorporate lipids and NADPH-dependent 172

protochlorophyllide oxidoreductase. Upon exposure to light, the prolamellar body disperses, 173

thylakoid membranes form coinciding with greening due to chlorophyll biosynthesis, and a 174

fully functional chloroplast develops. In light, proplastids in subepidermal meristematic cells 175

differentiate into green chloroplasts in the cotyledons (reviewed in Jarvis and Lopez-Juez, 176

2013). In linear monocot leaves, a gradient of chloroplast differentiation can be observed in 177

detail from the base of the leaf near the meristem where young cells contain proplastids, to 178

the older cells towards the tip that contain differentiated chloroplast (Li et al., 2010; Majeran 179

et al., 2010). Based on these observations, three different chloroplast developmental phases 180

have been defined: a heterotrophic phase of cellular proliferation and growth; a transition 181

phase of chloroplast biogenesis where proteins such as the plastid translation apparatus and 182

plastid enzymes accumulate; and a maturation phase of photosynthetic protein accumulation 183

and photosynthetic activity. Similar phases take place during dicot leaf development, 184

although their spatial distribution is not as distinct (López-Juez et al., 2008; Charuvi et al., 185

2012; Dubreuil et al., 2017). During biogenesis, the photosynthetic pigments chlorophylls 186

and carotenoids are synthesized through activation of the NADPH- dependent 187

protochlorophyllide oxidoreductase (POR) that converts protochlorophyllide into 188

chlorophyll, and the PSY central carotenoid biosynthesis gene (Toledo-Ortiz et al., 2010). 189

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Excessive accumulation of the chlorophyll precursor protochlorophyllide in the dark can 190

result in photooxidative damage (Reinbothe et al., 1996), which is minimized by the 191

photoprotective role of carotenoids during photosynthetic apparatus assembly (Niyogi, 1999; 192

Walter and Strack, 2011). 193

Dark/light signaling pathways are tightly associated with chloroplast biogenesis. 194

During the heterotrophic phase in darkness, PIF1 and PIF3 are negative regulators of 195

chloroplast development, particularly of tetrapyrrole biosynthesis genes (Huq et al., 2004; 196

Stephenson et al., 2009), and transcriptionally suppress together with EIN3 (which is 197

stabilized by soil-pressure enhanced ET production, see Box 2) chloroplast development 198

genes (Liu et al., 2017). Among these are the transcription factors GOLDEN2-LIKE 1 199

(GLK1) and GLK2, which are necessary for chloroplast development (Fitter et al., 2002; Oh 200

and Montgomery, 2014), and target genes involved in chlorophyll biosynthesis, light 201

harvesting, and electron transport (Waters et al., 2009). HY5, in contrast, promotes 202

chloroplast development during the light transition and early maturation phases (Lee et al., 203

2007). The PIF-HY5 regulatory module is essential to tightly regulate chloroplast 204

development and involves antagonistic activities of PIFs and HY5 as negative and positive 205

regulators, respectively, through direct binding to G-boxes of common targets (Chen et al., 206

2013; Toledo-Ortiz et al., 2014). Its relative activity is dynamically sensitive to dark, low 207

light, or higher light through modulation of PIF and HY5 abundance (Chen et al., 2013; 208

Toledo-Ortiz et al., 2014). Molecular evidence indicates that PIF and HY5 coexist and can 209

form bHLH/bZIP heterodimers. In the dark, PIF1/PIF3 are abundant whereas HY5 (and its 210

homologue HYH) are instable (Box 1), and thus the module activity is essentially repressive. 211

In low light, HY5/HYH are stabilized (Box 1) and form heterodimers with PIF1/PIF3, which 212

might function as inactive forms. Under higher light conditions, PIF1/PIF3 are almost 213

completely degraded and HY5/HYH become more prevalent, activating transcription of 214

common PIF-HY5 module targets (Chen et al., 2013). PIF-HY5 prevent protochlorophyllide 215

overaccumulation, control ROS signaling pathway, and regulate pigment accumulation 216

through directly binding to G-box motifs in the promoters of POR genes, ROS responsive 217

genes, and PSY and other central carotenoid and chlorophyll pathway genes (Toledo-Ortiz et 218

al., 2010; Chen et al., 2013; Toledo-Ortiz et al., 2014). 219

Fully developed chloroplasts are essential for the fixation of energy from sunlight, 220

and in turn function as light signalling structures with great impact on photomorphogenesis 221

through close coordination between the nucleus and chloroplast genomes. In Arabidopsis, 222

chloroplast retrograde signals from the chloroplast to the nucleus are able to optimize 223

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photosynthetic capacity and growth, prevent photodamage in high light environments and 224

fine-tune circadian regulated processes by releasing light-specific signals (Waters et al., 225

2009; Martín et al., 2016a; Dubreuil et al., 2017) (Box 3). 226

227

The hypocotyl 228

To quickly reach for the light, the elongated hypocotyl of dark-germinated seedlings is the 229

most remarkable phenotype. The Arabidopsis hypocotyl is an intensively studied model in 230

seedling etiolation and de-etiolation. The hypocotyl consists of a set number of 20 cells, and 231

elongation thus mainly dependents on cell expansion, rather than divisions (Wei et al., 1994; 232

Gendreau et al., 1997), and requires the uptake of water to maintain turgor pressure (Ishikawa 233

et al., 2013; Chaumont and Tyerman, 2014). To facilitate cell expansion, the cell wall of the 234

epidermal cells gains flexibility, which appears to be independent of cell wall synthesis, and 235

is regulated by specialized proteins such as expansins and XYLOGLUCAN 236

ENDOTRANSGLUCOSYLASE /HYDROLASEs (XTH’s) (Ivakov et al., 2017). In dark 237

conditions, PIFs directly induce the expression of the genes encoding for these proteins 238

(Leivar et al., 2009), and integrate the strong influence of several hormones such as auxin, 239

BRs, GA and ET in hypocotyl elongation (Box 2, reviewed in Leivar and Monte, 2014; de 240

Wit et al., 2016) (Fig. 3C). Auxin accumulates in the cotyledons and is actively transported 241

towards the hypocotyl, where PIN proteins locate it to the epidermal cells (Box 2). Auxin 242

acidifies the cell walls, which favors expansin and XTH-mediated elongation, and enhances 243

expression of the genes encoding for these proteins (Rayle and Cleland, 1992; Paque et al., 244

2014). The dwarf phenotype of dark-grown BR-deficient mutants (e.g. de-etiolated2 (det2)) 245

pointed out the important role of these steroid hormones in hypocotyl elongation during 246

skotomorphogenesis (Chory et al., 1991; Li et al., 1996). Recently it became clear that the 247

main function of BRs during elongation (in response to darkness, shade and high 248

temperatures) is indirect via the binding of BR-stabilized protein BZR1 to PIF4 (Box 2; Oh et 249

al., 2012). PIFs and BZR1 induce GA synthesis, which indirectly enhances hypocotyl growth 250

by inhibition of the repressing DELLA proteins (Box 2). In darkness, under mechanical 251

pressure created by soil, ET accumulates and inhibits hypocotyl growth, to strengthen the 252

hypocotyl (Box 2; Yu and Huang, 2017). As an additional level of signaling, elongating cell 253

walls release fragments which trigger a forward-loop and enhance skotomorphogenesis in the 254

hypocotyl and cotyledons (Sinclair et al., 2017). 255

Upon light exposure, hypocotyl elongation is quickly inhibited. Light-activated 256

photoreceptors cause PIF degradation and COP1 inactivation, which brings down hormone 257

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levels and releases growth-suppressing proteins such as HY5 (Box 1, 2). PHYs are expressed 258

plant-wide in different organs and tissues, but can play different roles in different cell layers. 259

A recent study shows how epidermal phyB is completely responsible for light-induced 260

germination and hypocotyl growth arrest in red light (Kim et al., 2016). Not much is known 261

about the role of other hypocotyl cell layers in growth (arrest) during seedling establishment. 262

Nevertheless, another recent study supports the cell-type specific functions in Arabidopsis 263

hypocotyls. Trichoblasts form hair-like structures and acquire nutrients from the external 264

environment, while the neighbouring atrichoblasts provide shortcut routes for these nutrients 265

to be unloaded and moved up the stem (Jackson et al., 2017). 266

267

The roots 268

When a seed germinates underground, reaching the light seems top priority, and this goes at 269

the cost of root development. To regulate this shoot-over-root trade-off, root development in 270

dark-grown seedlings is actively repressed. Auxin availability in the roots is strongly limited. 271

The suppression of PIN gene expression in the hypocotyl and the localization of PIN proteins 272

into the vacuole, both COP1-dependent, inhibit polar auxin transport (PAT) and thus root 273

growth (Box 2; Sassi et al., 2012) (Fig. 3D). Even though the roots will remain in close-to-274

dark conditions throughout the plant life cycle, light-perception by the shoot dramatically 275

affects root development (Gelderen et al., 2017; Lee et al., 2017). When the shoot 276

experiences light, COP1 is mobilized out of the nucleus and this releases the suppression of 277

the PIN proteins and activates PAT. Like many other aspects of seedling establishment in the 278

light, root development greatly dependents on HY5. The role for HY5 in Arabidopsis root 279

development has been known for a long time, as HY5-deficient mutants show defects in root 280

hair development, gravitropism, lateral root outgrowth and elongation (Oyama et al., 1997; 281

Sibout et al., 2006). The HY5 protein is, as was discovered recently, translocated via the 282

phloem towards the root, with root-specific HY5 and HYH transcription, and promoted root 283

development as a consequence (Chen et al., 2016; Zhang et al., 2017) (Fig. 3D). In addition 284

to HY5 being a traveling molecule, another recent study showed that its stability and 285

transcription is induced by stem-piped light that locally activates PHYB molecules in the 286

Arabidopsis roots (Lee et al., 2016). Besides auxin and HY5, sugar molecules travel from the 287

light-exposed cotyledons, which started photosynthesis, to the roots, and enhance root 288

elongation (Kircher and Schopfer, 2012) (Fig. 3D). By quickly enhancing root elongation and 289

lateral root outgrowth upon seedling establishment, the young photoautotrophic plant can 290

start the uptake of water and nutrients such as nitrate to fuel growth (Chen et al., 2016). 291

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292

Seedling establishment in alternating light/dark cycles 293

Upon seedling exposure to sunlight after germination, establishment proceeds under 294

light/dark cycles of variable duration and light intensity depending on the latitude and time of 295

the year. This section reviews our current knowledge on how seedling growth in these 296

conditions integrates light and dark signals with the circadian clock, which is synchronized 297

and oscillates strongly after light exposure (Salomé et al., 2008). 298

In photoperiodic conditions, growth is dark-dependent and promoted by accumulation 299

of the PIFs, similar to etiolated growth. Noteworthy, acceleration of hypocotyl elongation in 300

photoperiodic conditions is not linear as a function of the duration of the dark period, but 301

instead is a short day (SD)-specific event. Up to approximately 12 hours of darkness, 302

Arabidopsis hypocotyls are as short as if they were in constant light, and then elongation 303

increases with longer nights (Niwa et al., 2009) (Fig. 4). Mutants in the central clock 304

components CCA1ox or prr5prr7prr9 exhibit a nearly linear growth pattern in increasing 305

night lengths (Niwa et al., 2009), indicating that the circadian clock inhibits growth in 306

photoperiodic conditions. Whereas hypocotyl growth in the dark can be considered clock 307

independent, seedling establishment in light/dark cycles requires the integration of clock and 308

dark/light signaling to regulate elongation, cotyledon development and greening. 309

Regulation of hypocotyl elongation in light/dark cycles offers an example of the 310

intricate combined action of dark, light and clock signaling. In SD, PIF proteins control 311

rhythmic growth by collectively promoting increased elongation rates in the predawn hours 312

when they are most abundant. As a consequence, pifq seedlings are shorter than wild type in 313

SD, a difference that is less apparent in long days (LD), when nights are too short to allow for 314

strong PIF accumulation (Fig. 4). PIF accumulation and activity is regulated at several levels. 315

First, PIF4 and PIF5 transcripts in SD rise at midday through the night, with a peak at dawn 316

(Nozue et al., 2007). This oscillation is imposed by the evening complex (EC) formed by 317

ELF3, ELF4, and LUX (Nusinow et al., 2011), and by TOC1, PRR5 and PRR7 (Yamashino 318

et al., 2003; Niwa et al., 2009) that repress PIF4 and PIF5 expression during the day and 319

early night. PIF7 transcript levels oscillate as well, suggesting clock regulation (Kidokoro et 320

al., 2009; Lee and Thomashow, 2012). In contrast, PIF1 and PIF3 transcription is maintained 321

at a low and constant level during the diurnal cycle (Soy et al., 2012; Soy et al., 2014). 322

Second, as a consequence of phy activity, PIF protein abundance in SD oscillates diurnally 323

with low PIF levels during the light hours and progressive accumulation during the dark to 324

peak at dawn (Nozue et al., 2007; Soy et al., 2012; Yamashino et al., 2013). During the first 325

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night hours, phyB Pfr persists and inhibits PIF accumulation while slowly dark reverting to 326

inactive Pr (Sweere et al., 2001; Rausenberger et al., 2010; Medzihradszky et al., 2013). The 327

photoactivated phyB Pfr forms dynamic nuclear photobodies together with Hemera (HMR) to 328

induce rapid phosphorylation of PIFs leading to their degradation (Kircher et al., 2002; Chen 329

et al., 2010; Van Buskirk et al., 2014). phyB is also found in tandem zinc knuckle/plus3 330

(TZP)-dependent photobodies which also contain members of the EC (Kaiserli et al., 2015; 331

Huang et al., 2016a; Huang et al., 2016b), but apparently not HMR, which could indicate the 332

existence of specialized phyB-containing photobodies that might regulate PIF accumulation 333

or transcription separately. As a result of phy-imposed action, PIF1, PIF3, PIF4, and PIF5 334

abundance oscillates in SD to peak at dawn and induce growth-related genes (Nozue et al., 335

2007; Nozue et al., 2011; Nomoto et al., 2012; Soy et al., 2012; Yamashino et al., 2013; Soy 336

et al., 2014). Last, the growth-promoting activity of PIFs, as they progressively accumulate 337

during postdusk darkness, is directly inhibited by PIF-interacting clock components to 338

prevent detrimental early growth. The transcriptional-activator activity of PIFs is directly 339

repressed by TOC1 during postdusk, when TOC1 is most abundant in the circadian cycle 340

(Soy et al., 2016; Zhu et al., 2016). In addition, DNA binding of at least PIF4 is inhibited by 341

ELF3 in an EC-independent manner (Nieto et al., 2015). Thus, whereas the dark promotes 342

accumulation of the PIFs, the integration and convergence with the circadian clock limits the 343

timing of maximum responsiveness to dawn (Allen et al., 2006). This permissive gating 344

involves phasing of downstream effector transcript abundance (Covington et al., 2008; 345

Michael et al., 2008; Martín et al., 2016b) and calculation of the rate of starch breakdown to 346

ensure lasting energy to fuel growth at dawn (Graf et al., 2010). 347

348

Aboveground challenges delay seedling establishment 349

Even though germination is in a lot of plant species properly timed by external (humidity, 350

temperature, light) and internal (circadian rhythmic) cues, the above ground environment 351

often appears sub-optimal for a young establishing seedling. A combination of stresses will 352

inhibit or postpone photomorphogenic development during the dark-to-light transition or in 353

diurnal conditions. In this section, we will review the most studied external factors (excessive 354

light levels, light quality, neighbor detection, and high temperatures) that, to more or less 355

extent, inhibit the photomorphogenic phenotype to protect the seedling and escape harmful 356

situations. 357

Light intensity. Coming from a (close to) dark environment underground, the first 358

light seen by the de-etiolating seedling can cause problems. Excessive light levels are 359

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detrimental for plants and cause damage to the photosystem, resulting in ROS accumulation. 360

PHYs, CRYs, PHOTs and UVR8 selectively monitor for changes in light quality and small 361

changes in fluence rate. Nevertheless, photoreceptor activation saturates, and is insensitive 362

for extremely high, possibly damaging light intensity. As mentioned above, the chloroplasts 363

can sense and process information about the light intensity (see also Box 3). In high light 364

levels, RS inhibits the transcription of photomorphogenic genes involved in photosynthesis 365

and development. As a consequence, young seedlings that are shifted from darkness to a high 366

light environment have long hypocotyls and keep their cotyledons closed, to protect them and 367

the shoot apical meristem from the damaging light levels. Major players in the high-light 368

mediated RS are the plastid-localized PRR protein GENOMES UNCOUPLED1 (GUN1) and 369

ABI4 (Koussevitzky et al., 2007; Martín et al., 2016a; Xu et al., 2016). 370

Light quality and neighbor-induced competition. Above the ground, seedlings are 371

often not alone. The presence of neighboring plants can threaten light availability, and thus 372

photosynthesis rates. To prevent being completely shaded, most seedlings of sun-loving 373

plants will partly inhibit photomorphogenesis. The shade avoidance syndrome (SAS) triggers 374

hypocotyl elongation, despite the availability of light, and this way reach the top of the 375

canopy. This response is triggered by the low ratio between R and FR light, caused by the 376

preferential absorption of R and reflection of FR light by green tissues, and is enhanced when 377

additional B light depletion occurs during more severe shading (Filiault and Maloof, 2012; 378

Kohnen et al., 2016; de Wit et al., 2016b). The low R : FR light signal inactivates PhyB and 379

will thus keep the main PIFs acting in SAS (PIF4, 5 and 7) active (Lorrain et al., 2008; Li et 380

al., 2012) and the production of growth-promoting hormones such as auxin, BR, GA and ET 381

high (Li et al., 2012; Bou-Torrent et al., 2014). In young seedlings, the SAS consists of a 382

delay of some aspects of photomorphogenesis (hypocotyl growth arrest, cotyledon expansion, 383

root development, pigment accumulation), and promotes cotyledon petiole elongation and 384

upward cotyledon positioning (reviewed by Ballaré and Pierik, 2017; Fiorucci and 385

Fankhauser, 2017). In dense canopies, the emission of all kinds of volatile compounds 386

increases and they accumulate due to reduced airflow (Kegge et al., 2013). As most important 387

signaling volatile, in the light ET enhances elongation growth, in order for to reach the top of 388

the canopy. ET enhances PIF3 expression and, via similar regulatory pathways as shade 389

perception, synthesis and signaling of the growth promoting hormones auxin, GA and BR 390

(Zhong et al., 2012; Das et al., 2016). Interestingly, although some aspects of 391

photomorphogenesis are clearly suppressed by ethylene (hook unfolding and cotyledon 392

expansion, see above), others strongly depend on the light availability (hypocotyl elongation: 393

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suppressed in darkness, while induced in light) (Pierik et al., 2006). Another stress-full light 394

signal is UV-B radiation, which can cause DNA damage. Interestingly, in low quantities, 395

UV-B radiation perceived by the UVR8 receptor strongly enhances photomorphogenesis. It 396

is, most probably, used by plants as a signal for reaching the sunlight and suppresses the 397

elongated response of seedlings grown in shade (Hayes et al., 2014), via inhibition of COP1-398

mediated HY5 and HYH suppression (Favory et al., 2009; Rizzini et al., 2011; Christie et al., 399

2012). 400

High temperatures. With temperatures rising due to global climate change, heat is a 401

more and more relevant stress for plants. Small changes in temperature, sensed by PhyB and 402

phototropins (Jung et al., 2016; Legris et al., 2016; Fujii et al., 2017), partly inhibit 403

photomorphogenesis in young seedlings. This so called thermomorphogenic response 404

includes elongated hypocotyls and epinastic cotyledons and serves to enhance cooling of the 405

young leaves and thus warmth adaptation (reviewed in Van Zanten et al., 2014; Quint et al., 406

2016). The key-factor in this warmth-mediated arrest on de-etiolation is PIF4. The 407

inactivation of phys by high temperatures stabilizes the protein (Jung et al., 2016; Legris et 408

al., 2016), but also triggers COP1-mediated degradation of HY5, which releases the 409

suppression of PIF4 expression (Delker et al., 2014). High temperature-stabilized PIF4 will 410

continue to keep auxin synthesis high and hypocotyl elongation going, despite the light 411

availability (Franklin et al., 2011). The direct effect of other climate related stresses such as 412

drought and humidity on seedling photomorphogenesis, are less well understood. 413

Nevertheless, it is well-known that these contrasting stresses strongly affect the synthesis of 414

the phytohormone abscisic acid (ABA) (Christmann et al., 2007; Okamoto et al., 2008; Bauer 415

et al., 2013), which in turn interferes with light-induced development (Pierik and Testerink, 416

2014). 417

418

Concluding remarks 419

Plants have evolved sophisticated photoperception mechanisms to interpret their 420

environmental conditions and optimally coordinate and adjust their growth to thrive as sessile 421

organisms. Here we have reviewed how the relative dark and light signaling flux impacts 422

several processes during seedling establishment, with a focus on the growth programs in the 423

dark, upon first exposure to light, and in diurnal conditions where dark and light alternate. 424

Because seedlings are exquisitely sensitive to and actively respond to darkness and different 425

light intensities, we propose that seedling establishment is a dimmer-type switch-regulated 426

process between dark and light signals. This allows plants to dynamically respond to the 427

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relative amounts of dark and light signaling to optimize development. Research efforts over 428

the last decades have contributed to impressive progress in our understanding of seedling 429

establishment, especially in Arabidopsis. As the scientific community in the field makes new 430

discoveries, new exciting questions arise, and challenges are still many. We have summarized 431

a few important questions for future research in the “Outstanding questions” Box. We believe 432

novel emerging and enhanced technologies for high-throughput organ, tissue and single cell -433

omics, cell-cell, macromolecule- and organelle-level research (Nito et al., 2015), together 434

with cross-disciplinary approaches, will inspire and advance our tasks ahead. 435

436

Acknowledgements 437

We thank Gloria Villalba and David Blasco for their help with growing the crop plant 438

species, and Gabriela Toledo-Ortiz for valuable comments on the manuscript. Funding was 439

provided by grants from the Spanish “Ministerio de Economía y Competitividad” (MINECO) 440

BIO2015-68460-P, and from the Generalitat de Catalunya 2014-SGR-1406 to E.M. We 441

acknowledge financial support by the CERCA programme/Generalitat de Catalunya and from 442

MINECO through the “Severo Ochoa Programme for Centers of Excellence in R&D” 2016-443

2019 (SEV‐ 2015‐ 0533)”. 444

445

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446 Figure Legends 447

448

Figure 1. Arabidopsis seedling establishment after the switch from dark to light. 449

Representative pictures of (A) two day old dark-grown seedlings exposed to (left to right) 0h, 450

2h, 6h or 24h of low light (approximately 5 μmol m-2

s-1

PAR), and three day old (B) dark- 451

and (C) light-grown seedling. Scale bar = 2 mm. 452

453

Figure 2. Photomorphogenesis amongst crop species. Representative pictures of tomato 454

(Solanum lycopersicum), quinoa (Chenopodium quinoa) and sorghum (Sorghum bicolor) 455

seedlings, grown (from left to right) for two days in the dark exposed to 0h, 6h or 24h of low 456

light (approximately 5 μmol m-2

s-1

PAR), and for three days in the dark. Scale bars are 1 cm. 457

458

Figure 3. Dark- and light signaling induce organ-specific developmental traits in 459

Arabidopsis seedlings. Simplified representation of the traits that accompany development 460

in the dark (left panels) and upon first light signaling (right panels). For each organ (apical 461

hook, A; cotyledons, B; hypocotyl. C; and root, D) the most important regulatory factors are 462

shown. Schematic seedling cartoons are modified from the pictures in Fig.1. 463

464

Figure 4. Night length strongly affects photomorphogenesis in Arabidopsis seedlings. 465

Hypocotyl length (mm) of 3 day-old Arabidopsis wild-type (Col-0) and pifq (pif1-1 pif3-3 466

pif4-2 pif5-3; Leivar et al. 2008) seedlings, grown in continuous white light (WLc), long days 467

(LD; 16h L / 8h D), short days (SD; 8h L / 16h D) or continuous dark (Dc). Above the graph 468

are pictures of representative seedlings in the same order. All were grown in continuous 469

temperature (22ºC) and a light intensity of approximately 5 μmol m-2

s-1

PAR. Scale bar = 2 470

mm. 471

472

Box 2 Figure. Simplified schematic representation of hormone functions downstream of 473

dark/light signaling components. 474

475

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ADVANCES

• Dark and light signaling are interconnected and balanced during seedling emergence and day/night cycles.

• Photoreceptor-regulated transcription factors like PIFs and HY5 regulate seedling establishment through the regulation of 20% of the transcriptome in Arabidopsis.

• Cross-talk and integration between endogenous and light signaling pathways are necessary to optimize seedling establishment.

• Chloroplast-to-nucleus retrograde signaling impacts seedling establishment in high light conditions to protect from photo damage.

• Organ-specific and long-distance traveling signals are emerging as sophisticated regulatory mechanisms in the life of plants.

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OUTSTANDING QUESTIONS

• Is cell-specificity of key factors like PIFs, HY5, or hormones a regulatory mechanism in photomorphogenesis? Can they move to and / or accumulate in different cell types to coordinate rapid and local cellular responses to light?

• How does below-optimal seedling establishment affect growth and (crop) yield in later stages of plant development?

• How do environmental factors perceived underground before light exposure, such as temperature, soil minerals and water availability, affect seedling establishment?

• What are the composition and dynamics of dark and light-sensitive regulatory protein complexes?

• How are the relative amounts of dark and light signaling translated into transcriptional and biochemical responses?

• How is chloroplast retrograde signaling integrated with dark, light, and circadian clock signals to regulate development?What is the role of FIS1 homologs in plants? Do FIS1 homologs in animals have roles similar to those in plants?

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BOX 1. Perceiving and Signaling Dark and

Light: Receptors and Primary Regulators

The relative amount of light and dark modulates the flow of information signaled through a variety of wavelength-specific photoreceptors to their downstream signaling partners. UVR8 perceives Ultra Violet B light (UVB; 280-315 nm), phototropins (PHOT), cryptochromes (CRYs) and zeitlupe (ZTL) account for UV-A, blue, and green light (±315–550 nm) perception, and phytochromes (phyA-E) are sensitive for red (R) and far-red (FR) light (±600–750 nm). These photoreceptors regulate similar and distinct developmental transitions or adaptations in response to changing light environments (Galvão and Fankhauser, 2015). Seedling photomorphogenesis and establishment are mainly under control of phyB and phyA, and blue-light-activated CRY1 and CRY2. Active phys form nuclear photobodies mediated by HEMERA (HMR) or tandem zinc knuckle/plus3 (TZP) to centralize destabilization and transcription of photomorphogenesis-inhibiting proteins (Chen et al., 2010; Kaiserli et al., 2015; Huang et al., 2016b). The bHLH PHYTOCHROME INTERACTING FACTORS (PIFs) are transcription factors inhibited by light-activated phys and CRYs that repress photomorphogenesis and regulate many phytohormone pathways (Leivar and Monte, 2014; Ni et al., 2014; Pedmale et al., 2016; Dong et al., 2017a; Ni et al., 2017; reviewed in this focus issue by Pham et al., 2017). DELLA proteins create another inhibition level by preventing PIF

promotor binding in the light (de Lucas et al., 2008; Feng et al., 2008). Supporting the key-role of PIFs during seedling establishment, the pif-quadruple mutant (pifq; pif1pif3pif4pif5) is photomorphogenic in darkness and shorter in photoperiodic growth conditions (Bae and Choi, 2008; Leivar et al., 2008; Fig. 4).

Partially synergistically with PIFs act the central inhibitors of light signaling CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1) and DE-ETIOLATED1 (DET1; Dong et al., 2014; Xu et al., 2014). COP1 is a ubiquitin E3 ligase, which targets the photomorphogenesis-promoting transcription factors ELONGATED HYPOCOTYL 5 (HY5), HY5-HOMOLOGUE (HYH), and LONG HYPOCOTYL IN FAR RED (HFR1) in darkness (Osterlund et al., 2000; Yang et al., 2005). COP1 acts in a complex with SUPPRESSOR OF PHYA (SPA) proteins (Hoecker, 2017). Active PHYs and CRYs disassociate SPAs from COP1, releasing the suppressed proteins and causing export of COP1 from the nucleus (Pacin et al., 2014). DET1 is part of the CDD complex, together with COP10 and DAMAGED-DNA BINDING PROTEIN 1 (DDB1), which interacts with the CUL4 E3 ligase machinery. The CUL4-CDD complex suppresses photomorphogenesis by enhancing the COP1-SPA-mediated inhibition of HY5 and by stabilizing PIFs in the dark (Osterlund et al., 2000; Dong et al., 2014).

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BOX 2. Hormonal Regulation of Seedling

Photomorphogenesis

Auxin, brassinosteroids (BRs), gibberellic acid (GA), and ethylene (ET) are key regulators of photomorphogenesis and are under tight control of dark/light signaling components like PIFs, COP1 and HY5 (Box 1; Lau and Deng, 2010; Leivar and Monte, 2014; Lucas and Prat, 2014; Chaiwanon et al., 2016; de Wit et al., 2016a).

Auxin locally induces growth and can be transported from the shoot towards the hypocotyl and roots. PIFs induce auxin synthesis (Hornitschek et al., 2012; Pfeiffer et al., 2014) and downstream signaling factors (AUXIN RESPONSE FACTORS [ARFs], INDOLEACETIC ACID-INDUCIBLE [AUX/IAA] and SMALL AUXIN UPREGULATED [SAUR] genes), while auxin influx (AUXIN1 [AUX1] and LIKE-AUX1 [LAX]) and efflux (PIN-LIKE [PIN]) proteins account for polar auxin transport. In dark-grown seedlings, PIN4 and PIN7 create the auxin gradient that causes the apical hook (Fig. 3; Žádníková et al., 2016). Dark-active COP1 suppresses PIN1 transcription in the shoot and PIN1/2 polar localization in roots, resulting in low auxin levels in the root system (Fig. 3; Sassi et al., 2012).

BRs are essential for skotomorphogenic growth, proven by the cop-like phenotype of DE-ETIOLATED2 (DET2) deficient mutants impaired in BR synthesis (Li et al., 1996). BR does not accumulate in darkness (Symons et al., 2002), but PIF4 function greatly depends on dimerization with the BR-stabilized BRASSINAZOLE-RESISTANT 1 (BZR1). The PIF4-BZR1 module induces auxin signaling, and BR and GA synthesis (Oh et al., 2012; Oh et al., 2014; Shahnejat-Bushehri et al., 2016). In light, BZR1 interacts with HY5, which

subsequently makes BRs regulators of photomorphogenis (Li and He, 2016).

In darkness, PIF induction of GA synthesis activates the GIBBERELLIN INSENSITIVE DWARF 1 (GID1) receptor, which subsequently targets DELLA proteins for degradation. DELLA proteins act, in the absence of GA, as repressors of PIFs and BZR1 (Feng et al., 2008; de Lucas et al., 2008; Shahnejat-Bushehri et al., 2016).

ET is induced by PIFs and accumulates when seedlings experience pressure by a soil column. ET and COP1 destabilize the F-BOX proteins EIN3 BINDING FACTOR 1 and 2 (EBF1 and 2), suppressors of ETHYLENE INSENSITIVE 3 (EIN3). In darkness, ET induces the triple response (thick hypocotyl, exaggerated hook, short root; Guzman and Ecker, 1990), which strengthens the seedling and protects the meristem during soil outgrowth. In return, EIN3 induces PIF3 expression (Zhong et al., 2012). In light, phyB stimulates EBF1/2 mediated EIN3 and PIF3 degradation, and ET signaling is inhibited (Jeong et al., 2016; Shi et al., 2016; Dong et al., 2017b).

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BOX 3. Chloroplast-to-Nucleus Retrograde

Signaling

The chloroplast genome, or plastome, carries fewer than 100 protein-coding genes. The majority of chloroplast proteins (~2000–3000) are encoded by the nucleus and are imported into the chloroplast following synthesis in the cytosol. This nucleus-to-chloroplast signaling is termed anterograde signaling. Chloroplasts are well known as the organelles where photosynthesis is performed, but they are also dynamic signaling compartments that function as intracellular and environmental sensors. They can communicate with the nucleus through a process termed retrograde signaling (RS) to regulate expression according to chloroplast status. In developing chloroplasts, RS coordinates photosystem assembly and maintenance with the other processes required for chloroplasts biogenesis (biogenic RS). Once mature, chloroplasts communicate with the nucleus to maintain homeostasis in the prevailing environment (operational RS; Chi et al., 2013; Jarvis and Lopez-Juez, 2013; Noren et al., 2016).

During chloroplast development, use of lincomycin or norflurazon to inhibit plastid translation or carotenoid biosynthesis,

respectively, leads to photobleaching and repression of photosynthesis-associated nuclear genes (PhANGs), such as those from the chlorophyll-binding LHCb gene family. genomes uncoupled (gun) mutants exhibit PhANG derepression in response to norflurazon and have helped elucidate components of biogenic signaling, such as heme, tetrapyrroles, and GUN1 (Koussevitzky et al., 2007). Other key components include chloroplast-localized PLASTID REDOX INSENSITIVE2 (PRIN2) and plastid-encoded RNA polymerase (PEP; Kindgren et al., 2012), and nucleus-localized ABI4 and GLKs (Koussevitzky et al., 2007; Kakizaki et al., 2009; Waters et al., 2009).

On the basis of the phenotypes of plants with disrupted plastid functionality, RS has been shown to impact normal light-regulated development. Whereas light at moderate levels acts through the phy sensory-photoreceptor system to induce photomorphogenic development, light at excessive levels is sensed by the plastid and represses photomorphogenesis through a GUN1-mediated RS mechanism independent of PIF mediation (Ruckle and Larkin, 2009; Martín et al., 2016a).

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