update on photomorphogenesis - plant physiology...2017/12/07 · 1406 to e.m. we acknowledge financ...
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Update on Photomorphogenesis 1
Seedling establishment: a dimmer switch-regulated process between dark 2
and light signaling 3
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Charlotte M. M. Gommers and Elena Monte* 5
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*Author for correspondence 7
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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
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Short title: Dark and light signals shape seedling establishment 13
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Corresponding author: Elena Monte, [email protected] 15
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Author contributions: C.M.M.G and E.M. wrote the manuscript, C.M.M.G. composed the 17
figures. 18
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Single sentence summary: A balance between dark and light signaling directs seedling 20
establishment through integrating internal and environmental information. 21
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The authors declare no conflict of interest. 23
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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
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Corresponding author e-mail: [email protected] 31
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Plant Physiology Preview. Published on December 7, 2017, as DOI:10.1104/pp.17.01460
Copyright 2017 by the American Society of Plant Biologists
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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
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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
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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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12
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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13
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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14
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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15
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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16
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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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