Light signaling, root development and plasticity · 2 Light signaling, root development and...

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Title: 1

Light signaling, root development and plasticity 2

Kasper van Gelderen1, Chiakai Kang1 & Ronald Pierik* 3 4 1These authors contributed equally 5 *Author for correspondence 6

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Author affiliation: 8

Plant Ecophysiology, Utrecht University. Padualaan 8, 3584CH Utrecht, the Netherlands. 9

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Short title: 11

Light signaling, root development and plasticity 12

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Corresponding author: Prof. Dr. Ronald Pierik, [email protected], Plant Ecophysiology, Utrecht 14

University. Padualaan 8, 3584CH Utrecht, the Netherlands 15

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Author contributions: K.v.G., C.K. and R.P. wrote the manuscript and composed the figures. 18

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Funding Information 20

K.v.G. is funded by the Netherlands Organisation for Scientific Research, open competition grant 21

823.01.013 to R.P., C.K. is funded by the scholarship of government sponsorship for overseas 22

study, Taiwan, admission number 0991167-2-UK-004. 23

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Single sentence summary 26

Light signaling can affect root development and plasticity, either direct, or through shoot-root 27

communication via sugars, hormones, light, or other mobile factors. 28

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Competing interests 30

The authors declare no competing interests 31

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Plant Physiology Preview. Published on September 22, 2017, as DOI:10.1104/pp.17.01079

Copyright 2017 by the American Society of Plant Biologists

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Corresponding author e-mail: 33

[email protected] 34

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Light is the energy source for plants as it drives photosynthesis to produce sugars. Given the 36

obvious fact that light mostly occurs aboveground and not in the soil, most interactions of plants 37

with light have been studied in shoot parts of the plant. Research over more than a century has 38

yielded tremendous insights into how light not only drives photosynthesis, but also acts as an 39

environmental cue that informs plants about their environment. Light quality and duration for 40

example, drive major developmental changes such as photomorphogenesis, photoperiodic 41

induction of flowering, phototropism, and shade avoidance (see for example the following recent 42

reviews: (Wu, 2014; Fankhauser and Christie, 2015; Xu et al., 2015; Ballaré and Pierik, 2017). 43

The picture that has emerged is that plants have very detailed light signaling mechanisms, with 44

photoreceptors dedicated to different wavelengths in the light spectrum and interactions between 45

these photoreceptors themselves and their downstream signal transduction pathways. 46

Studies have accumulated over the past 15 years, and intensified in recent years showing 47

pronounced effects of light on root physiology and development. Although some effects of light 48

availability on root growth will be the simple consequence of differential sugar availability to the 49

roots due to photosynthesis in the shoot, there is substantial evidence for more sophisticated 50

signaling impacts of different aspects of the light environment. 51

In this Update, we will briefly review the core light signaling mechanisms, their impact on root 52

development and plasticity and the functional implications of these above-belowground 53

interactions. 54

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LIGHT SIGNALING 57

Different wavelengths of light are associated with various functions in plant development and 58

plants have a range of photoreceptors to detect these wavelengths. UVR8 is sensitive to UV-B 59

light, cryptochromes (CRY) and phototropins (PHOT) detect UV-A and blue light, whereas 60

phytochromes (PHY) sense red (R) and far-red (FR) light. Photoreceptors occur all over the 61

plant body and although they are most abundant in the shoot, they are also expressed in the 62

roots (Fig. 1). Photoreceptors share downstream signaling hubs, notably the COP1/SPA 63

complex and PIFs, which will be discussed first, followed by the properties of each photoreceptor 64

group. 65

66

Shared signaling hubs 67

COP1-SPA-HY5 68



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CONSTIITUTIVE PHOTOMOPRHOGENESIS1 (COP1) functions as a ubiquitin E3 ligase that 69

targets proteins required for photomorphogenesis for degradation, such as the bZIP transcription 70

factor ELONGATED HYPOCOTYL 5 (HY5) (Osterlund et al., 2000; Saijo et al., 2003) and HY5-71

HOMOLOGUE (HYH) (Holm et al., 2002). Especially HY5 is a key regulator in 72

photomorphogenesis, and it serves as the center of a transcriptional network hub of hormone 73

and light signaling (Gangappa and Botto, 2016). Besides HY5, COP1 also targets factors like the 74

MYB transcription factor LONG AFTER FAR-RED LIGHT 1 (LAF1) (Seo et al., 2003), the bHLH 75

protein LONG HYPOCOTYL IN FAR-RED 1 (HFR1) (Duek et al., 2004) and even phytochrome 76

A (phyA) and phyB photoreceptors (Seo et al., 2004; Jang et al., 2010). COP1 activity relies on 77

physical interaction with SUPPRESSOR OF PHYTOCHROME A proteins (SPAs) in the COP1-78

SPA complex. The cryptochrome photoreceptors CRY1 and CRY2, upon blue light activation, 79

can bind to SPAs and this results in reduced COP1-SPA interaction, leading to stabilization of 80

COP1 targets (Lian et al., 2011; Liu et al., 2011; Zuo et al., 2011). Comparable interaction 81



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mechanisms exist between phytochromes and SPAs (Zheng et al., 2013; Sheerin et al., 2015), 82

and UVR8 and SPAs (Favory et al., 2009; Huang et al., 2013) Another mechanism that controls 83

COP1 activity is its light-based nuclear exclusion that affects HY5 degradation (von Arnim and 84

Deng, 1994; Pacin et al., 2014). COP1 and HY5 are well-known regulators of the transition from 85

skoto- to photomorphogenesis and for a detailed overview we refer to (Huang et al., 2014). 86

87

PHYTOCHROME INTERACTING FACTORS (PIFs) 88

PIFs are a group of basic helix-loop-helix (bHLH) transcription factors that mediate various 89

physiological responses, such as seed germination, seedling photomorphogenesis, shade 90

avoidance and shoot architectural responses to elevated temperature (Koini et al., 2009; Chen 91

and Chory, 2011; Hornitschek et al., 2012; Jeong and Choi, 2013; Xu et al., 2015). PIFs are 92

regulated by light, temperature and the circadian clock and these cues can lead to PIF 93

degradation by concerted action of the phytochromes and the E3-ligase Light-Response Bric-a-94

Brack/Tramtrack/Broad (BTB) (LRB) (Leivar and Monte, 2014; Ni et al., 2014; Jung et al., 2016; 95

Legris et al., 2016). The phytochrome and cryptochrome photoreceptors can physically interact 96

with specific sets of PIF proteins and thereby regulate PIF phosphorylation. The phosphorylation 97



6

status of PIFs subsequently determines their activity and in most instances their stability (Paik et 98

al., 2017). ChIP-seq studies on PIFs have identified a very broad range of target genes, 99

including those associated with cell wall modifications, auxin biology and several other 100

transcription factors. This broad range of targets combined with the multitude of signals that 101

impact on PIF stability makes PIF proteins a signaling hub to integrate environmental conditions 102

(Leivar and Monte, 2014; Paik et al., 2017). 103

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Photoreceptors 105

UV-B RESISTANCE LOCUS8 (UVR8) 106

The effect of UV-B radiation on plant growth is dual. High fluence UV-B exposure causes 107

photodamage, but low fluence UV-B contributes to photomorphogenesis and it increases the 108

resistance to herbivorous insects and pathogens (Ballaré et al., 2012; Galvão and Fankhauser, 109

2015). UV-B (280-315 nm) is perceived by UVR8, which uses a structure based on tryptophans 110

and a complex salt bridge network. Upon sensing UV-B light, the salt bridges are disrupted, 111

inducing dimer dissociation into UVR8 monomers and initiating signal transduction (Christie et 112

al., 2012). The UV-B induced responses include hypocotyl growth inhibition, altered leaf 113

morphogenesis, stomatal closure and compound synthesis associated with the prevention and 114

repair of UV damage (Binkert et al., 2014; Galvão and Fankhauser, 2015). UVR8 regulates UV-B 115

responses by negatively affecting COP1 function through the UVR8-SPA interaction (Osterlund 116

et al., 2000; Favory et al., 2009; Huang et al., 2013; Hayes et al., 2014). Formation of UVR8-117

SPA leads to inhibition of COP1 function and this results in stabilization of amongst others HY5 118

and HYH, thereby inducing genes downstream associated with UV-B signaling (Osterlund et al., 119

2000; Rizzini et al., 2011; Hayes et al., 2014). 120

121

Cryptochromes 122

Blue light (320-500 nm) is used for photosynthesis and also serves as a signal for shade, 123

photoperiodism and directional light. Blue light sensing is performed by three groups of light 124

receptors: cryptochromes, phototropins, and other LOV-domain containing receptors such as 125

ZEITLUPE. Cryptochromes (CRYs) are blue light receptors found in a broad range of organisms, 126

including bacteria, fungi, animals, and plants. Three CRYs are encoded in the Arabidopsis 127

genome, CRY1, CRY2, and CRY3. CRY1 and CRY2 act redundantly in promoting flower 128

induction, sensing blue light as input to circadian clock, and stomatal opening in Arabidopsis (Li 129

and Yang, 2007; Galvão and Fankhauser, 2015; Mo et al., 2015). Both CRY1 and CRY2 130

regulate primary root elongation, but CRY1 promotes primary root elongation in blue light, 131



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whereas CRY2 has the opposite effect (Canamero et al., 2006). Mainly CRY2 is expressed in 132

Arabidopsis roots (Fig. 1) and CRY1 and CRY2 inhibit root growth via modulation of free auxin 133

levels and polar auxin transport (Mo et al., 2015). The biological function of CRY3 is unclear yet 134

(Song et al., 2006; Klar et al., 2007; Mo et al., 2015). CRYs are nuclear flavoproteins, composed 135

of two domains, an N-terminal photolyase-related (PHR) region and a C-terminal domain of 136

varying size. The PHR region binds the chromophore FAD and serves as the light sensing part. 137

Upon absorbing blue/UV-A light, CRY is phosphorylated and can interact with other protein 138

partners, such as COP1, SPAs and PIFs (Lian et al., 2011; Liu et al., 2011; Zuo et al., 2011; 139

Pedmale et al., 2016; de Wit et al., 2016). 140

141

Phototropins 142

Phototropins are blue light receptors that mediate phototropism, chloroplast movement and 143

stomatal opening in Arabidopsis (Briggs and Christie, 2002). There are two phototropins 144

identified in Arabidopsis, phot1 and phot2, with similar function and structure. Besides their 145

function in the shoot, phot1 is also expressed in the roots, regulating root bending (Wan et al., 146

2012; Zhang et al., 2013). In contrast to other photoreceptors, which are present in the nucleus 147

or cytoplasm, phototropins are located in the plasma membrane (Sakamoto and Briggs, 2002). 148

When phot1 is activated by blue light, it phosphorylates PHYTOCHROME KINASE SUBSTRATE 149

4 (PKS4), and interacts with NON-PHOTOTROPIC HYPOCOTYL 3 (NPH3) to form a phot1-150

PKS-NPH3 protein complex (Pedmale and Liscum, 2007; Demarsy et al., 2012). This modulates 151

auxin transport and thus underlies plant phototropism (Fankhauser and Christie, 2015). Phots 152

have N-terminal flavin mononucleotide (FMN) chromophore-binding light oxygen voltage (LOV1 153

and LOV2) domains for light absorption, and a C-terminal AGC-type Ser/Thr protein kinase 154

signaling domain (Briggs and Christie, 2002). 155

The ZEITLUPE (ZTL), FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1), and LOV KELCH 156

PROTEIN2 (LKP2), are blue light photoreceptors involved in circadian clock and photoperiodic 157

flowering regulation, with a structure similar to Phots, but with only one LOV domain followed by 158

an F-box and six Kelch repeats (Galvão and Fankhauser, 2015). 159

160

Phytochromes 161

Phytochromes are photoreceptors sensing R and FR light that occur in plants as well as in fungi 162

and prokaryotes (Burgie and Vierstra, 2014). Plants use R/FR light signaling through 163

phytochromes to regulate germination, de-etiolation, stomatal development, flowering transition, 164

senescence, and shade avoidance (Franklin and Quail, 2010). Five phytochromes are identified 165



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in Arabidopsis, phyA-phyE. Phytochromes use the N-terminal covalently linked phytochromobilin 166

to sense light and the C-terminus to transmit the light signal. Phytochromes undergo reversible 167

conformation changes: The inactive Pr form absorbs R light (max=660nm) that leads to its 168

photoconversion into the active Pfr form that can then absorb FR light (max=730nm) to be 169

inactivated. Upon activation, Pfr translocates from the cytosol to the nucleus, where it interacts 170

with PIFs, modulating their activity (Chen and Chory, 2011; Leivar and Quail, 2011; Xu et al., 171

2015). PhyA, PhyB, PhyD and PhyE are expressed in the root, while PhyC expression in the root 172

is hardly detectable (Fig. 1). Phyb mutants have been shown to produce fewer lateral roots 173

(Salisbury et al., 2007) and Phyb and Phya single and double mutants have reduced root 174

elongation compared to wild-type (Correll and Kiss, 2005; Silva-Navas et al., 2015). Recently, 175

PhyB has been identified to act as a temperature sensor (Jung et al., 2016; Legris et al., 2016), 176

which is interesting since heat stress is known to lead to increased main root growth (Hanzawa 177

et al., 2013). If this occurs through PhyB signaling is yet to be resolved, but since high 178

temperatures destabilize PhyB and PhyB mutants have reduced root lengths, this may not be 179

likely. 180

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IMPACT OF DIRECT LIGHT SIGNALING ON ROOT DEVELOPMENT AND PLASTICITY 183

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Root development in dark versus light 185

Root development (Box 1) starts at embryogenesis (Scheres et al., 1994) and all root layers are 186

continuously formed from stem cells at the tip (Petricka et al., 2012) that are maintained by a 187

constant auxin flow (Blilou et al., 2005; Galinha et al., 2007; Stepanova et al., 2008; Mähönen et 188

al., 2014), while cytokinin promotes differentiation of these root layers (Dello Ioio et al., 2007; 189

Dello Ioio et al., 2008). Lateral roots form after embryogenesis and are primed in the 190

differentiation zone of the meristem (De Smet et al., 2007; De Rybel et al., 2010). Subsequently 191

they emerge through the outer layers of the main root (Lavenus et al., 2013) upon modifications 192

of these layers (Péret et al., 2013; Vermeer et al., 2014). In total darkness, the Arabidopsis 193

seedling elongates its hypocotyl in an attempt to penetrate the soil, however its root stays very 194

small (Fig. 2). Roots of dark-grown seedlings are much shorter and have a much thinner 195

diameter than those of light-grown seedlings (Laxmi et al., 2008; Dyachok et al., 2011). When 196

etiolated seedlings are exposed to light they inhibit hypocotyl elongation, develop their 197

cotyledons and start to photosynthesize (Wu, 2014). Cotyledon-derived sugars are essential for 198

the start of root growth and when young seedlings are decapitated root growth is slowed 199



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dramatically, also when grown in the light (Kircher and Schopfer, 2012). Besides sucrose, the 200

basipetal flow of auxin is necessary to facilitate root growth in seedlings (Bhalerao et al., 2002) 201

and in the dark this basipetal auxin transport is very low due to the depletion of PIN-FORMED 202

(PIN) auxin efflux carriers from the plasma membrane (Laxmi et al., 2008; Sassi et al., 2012). 203



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Light induces root growth by providing sugars and auxin to the young root and specifically red 204

and blue light exhibit a positive effect on root elongation when compared to darkness (Sweere, 205

2001; Canamero et al., 2006; Costigan et al., 2011)(Fig. 2). However, the addition of sucrose to 206

the agar medium can sometimes reverse this effect (Correll and Kiss, 2005). Supplementation of 207

white light with FR light reduces root growth compared to normal white light (Salisbury et al., 208



11

2007)(Fig. 2) and UVB has a strong inhibiting effect on root growth, either when supplied to the 209

whole seedling or only the root (Tong et al., 2008; Leasure et al., 2009; Silva-Navas et al., 2015) 210

Many experiments addressing root development have been performed in the presence 211

of light on the whole seedling since root development is typically studied in vertical agar plate 212

set-ups with transparent medium. In field conditions the top part of the root system will grow in 213

minimal light and the lower part will even develop in darkness, while the shoot can be exposed to 214

various different light conditions (Smith, 1982). Several solutions to these undesirable lab 215

conditions have been postulated, including dark agar plugs (Sassi et al., 2012), black-colored 216

vertical plates (Xu et al., 2013) and the D-root system consisting of plate inserts plus cover slips 217

(Silva-Navas et al., 2015). In the D-root system, seedlings grow on medium in vertical square 218

plates, but an insert at the root-shoot junction and an external cover slip prevents light exposure 219

of the roots, whereas the shoot is exposed to the ambient light conditions. Compared to plants 220

with roots grown in fully exposed light conditions, plants with roots in darkness have increased 221

main root length and lateral root number, while root hair length decreased. When dark-grown 222

roots were exposed to light for a duration longer than 8 hours, their growth rate and root 223

meristem size declined (Silva-Navas et al., 2016). Interestingly, shielding roots from light 224

decreased the sensitivity of the main root to the plant hormones abscisic acid (ABA), 225

brassinolide (BL) and 6-benzyladenine (BAP), while the sensitivity to indole-3-acetic acid (IAA) 226

was increased (Silva-Navas et al., 2015). Interestingly, dark-exposed roots were less sensitive to 227

salt- and low nitrogen conditions, compared to light-exposed roots (Silva-Navas et al., 2015). 228

These data show that direct perception of light by the root is physiologically relevant in 229

Arabidopsis seedlings. 230

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Light affects root developmental plasticity 232

The root system can change the direction of growth in response to stimuli such as gravity 233

(Morita, 2010) or light (Kutschera and Briggs, 2012). The movement of the root away from light 234

sources or ‘root negative phototropism’ is dependent upon blue-light perception by phototropins 235

(Wan et al., 2012). Contrary to the negative response to blue light, a positive growth response of 236

the root to red light has also been observed (Kiss et al., 2001), but this response is weak and 237

can only be observed in the absence of gravity sensing (Ruppel et al., 2001; Kiss, 2003). 238

Downstream of light perception, root phototropism impinges on elements involved in root 239

gravitropism (Kiss, 2003; Kutschera and Briggs, 2012). 240

241

Root-negative phototropism 242



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Root negative phototropism is induced by blue and white light and the photoreceptors involved 243

are mainly phot1 and phot2, with minor roles for phyA and cry1/cry2 (Boccalandro et al., 2007; 244

Wan et al., 2012; Silva-Navas et al., 2016). NON-PHOTOTROPIC HYPOCOTYL3 (NPH3), a 245

target of phot1 and phot2 involved in hypocotyl phototropism, is also an important player in root 246

negative phototropism (Wan et al., 2012). Downstream of directional light perception, polar auxin 247

transport directs auxin away from the illuminated side. This auxin transport gradient requires 248

rootward plasma membrane localization of the auxin efflux carrier PIN1 in the stele, lateral 249

relocalization of PIN3 in the columella and rootward relocalization of PIN2 in the epidermis (Wan 250

et al., 2012; Zhang et al., 2013; Zhang et al., 2014). The relocalization of PIN2 and PIN3 is 251

dependent upon the recycling and targeted degradation (vacuolar targeting) of these PIN 252

carriers from one side of the membrane to the other (Wan et al., 2012; Zhang et al., 2013). The 253

initial perception of gravitropism and phototropism is different, but the downstream signaling 254

events of negative phototropism are very similar to those found in root gravitropism, involving 255

comparable PIN protein and auxin transport dynamics (Friml et al., 2002; Abas et al., 2006; 256

Baster et al., 2012). Most root phototropism experiments have been performed under conditions 257

where the whole seedling was directionally illuminated. When roots, which had been grown in 258

the dark, were stimulated by a one-sided white-light stimulus, while the shoot still remained in 259

the dark, the negative phototropism persisted and an important role for flavonols was uncovered 260

in the regulation of this response (Silva-Navas et al., 2016). White light, together with cytokinins, 261

stimulates the accumulation of flavonols on the lighted side of the root, which induces cell 262

elongation and stimulates PIN1 plasma membrane abundance (Buer and Muday, 2004; Silva-263

Navas et al., 2016). 264

265

Interaction of light and gravitropism 266

As mentioned above, root-negative phototropism and gravitropism both rely on polar auxin 267

transport. Light influences the direction of polar auxin transport by controlling the plasma 268

membrane abundance of PIN proteins (Laxmi et al., 2008; Sassi et al., 2012; Wan et al., 2012; 269

Zhang et al., 2013; Zhang et al., 2014). An interesting example of how light interacts with the 270

gravitropic output is the U-turn that an inverted maize seedling root makes when growing in a 271

glass tube exposed to light (Burbach et al., 2012; Suzuki et al., 2016). When these seedlings are 272

inverted in the dark, they do not show this strong gravitropic response (U-turn), indicating that 273

light can increase gravitropism. In accordance with this, Arabidopsis root slanting (on agar 274

plates) and the root gravitropic response are reduced in the D-root system where roots are kept 275

in darkness (Silva-Navas et al., 2015). Light stimulates the gravitropic response through the 276



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increase of flavonol biosynthesis, which increases root auxin levels (Buer and Muday, 2004; 277

Silva-Navas et al., 2016). Interestingly, FR light enrichment of Arabidopsis seedlings grown fully 278

in the light leads to reduced activity of the auxin reporter pDR5::GUS (Salisbury et al., 2007), 279

showing how light quality can markedly change root auxin homeostasis. Another way that light 280

signaling influences auxin transport in the root is by controlling the removal of PIN proteins from 281

the plasma membrane via the process of vacuolar degradation. Since PINs are transmembrane 282

proteins, their degradation occurs through vacuolar targeting and subsequent degradation of 283

Multi-Vesicular-Bodies containing PINs (Korbei and Luschnig, 2013). This vacuolar degradation 284

of PINs is an important process in changing PIN polarity and is essential for the regulation of 285

gravitropism (Baster et al., 2012). PIN2-GFP vacuolar targeting is controlled by the COP1/CSN 286

complex in a light dependent manner (Laxmi et al., 2008; Sassi et al., 2012). When a seedling is 287

incubated in darkness for several hours PIN2-GFP is targeted towards the vacuole (Kleine-Vehn 288

et al., 2008), however this does not occur when only the seedling shoot is given a light 289

treatment, or in the cop1-6 mutant (Sassi et al., 2012), showing how (COP1-mediated) light 290

signaling in the shoot can affect root development. 291

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ABOVEGROUND LIGHT REGULATES ROOT DEVELOPMENT: MECHANISMS AND 294

CONSEQUENCES. 295

As mentioned above, it is critical to research the effects of light signaling on root developmental 296

plasticity under conditions where roots are not directly exposed to the light environment as they 297

are typically shielded from by the soil under natural conditions. Indeed, root systems develop 298

differently between dark and light conditions of the roots themselves. Since plants constantly 299

coordinate growth and development of root and shoot in response to their highly dynamic 300

environment, they do need to translate important information about their light environment to the 301

root system. This is of particular importance under dense planting conditions, such as in most 302

agricultural fields, where both above and below ground competition for resources occurs (Pierik 303

et al., 2013; Gundel et al., 2014). Belowground, plants compete for water and nutrients whereas 304

aboveground they struggle for light. Belowground competition is size-symmetric, which means 305

that resource acquisition is proportional to the size of the root system of a given individual in a 306

dense stand. Competition for light is size-asymmetric: A plant that is only slightly taller than its 307

neighbors can put its leaves above these neighbors, thereby severely limiting their total access 308

to light, whilst itself not being affected at all by its neighbors (Weiner, 1985; Weiner and Thomas, 309

1986). Aboveground, plants maximize their competitive performance against neighbors by 310



14

activating the so-called shade avoidance response (Box 2). Briefly, FR light reflected by 311

neighbor plants inactivates the phytochrome photoreceptors and this relieves their repression of 312

PIF 4, 5 and 7. PIFs then accumulate, induce auxin biosynthesis and transport, and auxin 313

subsequently induces elongation of hypocotyls, stems and petioles as well as upward leaf 314

movement (Lorrain et al., 2008; Keuskamp et al., 2010; Keuskamp et al., 2011; Casal, 2013; 315

Gommers et al., 2013; Kohnen et al., 2016; de Wit et al., 2016; Ballaré and Pierik, 2017; 316

Michaud et al., 2017; Pantazopoulou et al., 2017). In this section, we briefly review the currently 317

established mechanisms of light signal information transfer from the shoot to the root, followed 318

by a discussion on its functional importance under dense planting conditions and plant 319

competition. 320

321

Mechanisms of light signal information transfer from shoot to root 322

Stem-piped light 323

Stem-piped light refers to the light transmitted through the internal tissues of the plants from the 324

shoot to the root. This manner of light transmission through the interiors of the plant has been 325

described for woody and herbaceous species. Light piping is wavelength-specific and long 326

wavelengths such as FR and near infra-red light are transmitted relatively well while shorter 327

wavelengths such as blue and green light are less effectively transmitted (Sun et al., 2003; Sun 328

et al., 2005). Stem-piped light can activate root-expressed phyB, which on its turn regulates HY5 329

in the Arabidopsis root (Lee et al., 2016). HY5 is involved in root growth in response to light, 330

modulating e.g. root gravitropism and nitrogen uptake (Cluis et al., 2004; Lee et al., 2007; Huang 331

et al., 2015; Chen et al., 2016). Therefore, stem-piped light might communicate information 332

about the aboveground light environment to the root (Fig. 3). However, the light transmission 333

goes down to 1% when conduction distances increase to 3 cm in herbaceous plants (Sun et al., 334

2005), which suggests that this mechanism might play a relatively modest role in mature planting 335

systems. 336

337

Mobile (signaling) chemicals 338

Although various components are transported from the shoot to the root, only few of them have 339

been directly linked to light signaling in the shoot. These include sugars derived from 340

photosynthesis and transported through the phloem, plant hormones, and HY5. These will be 341

briefly discussed below. 342

343

Sugars 344



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Once a seed is germinated, it first invests energy in hypocotyl growth. Upon penetrating the soil 345

and perceiving light, photomorphogenesis is initiated and the seedling acquires the ability to 346

conduct photosynthesis, followed by root growth (Kircher and Schopfer, 2012). It was shown in 347

Arabidopsis seedlings that blocking photosynthesis inhibits root growth, just like in darkness, and 348

that adding sucrose to the growth medium can rescue root growth. Interestingly, sucrose 349

addition could not induce additional root growth in photosynthesis-positive seedlings (Kircher 350

and Schopfer, 2012). These data confirm that sucrose is needed for root growth and 351

development, and indicate that sucrose can serve as a long-distance signal from the shoot to 352

inform the root system about light availability aboveground (Fig. 3). 353

354

Auxin 355

Young shoot tissues are the main source of the plant hormone auxin that is then transported to 356

the root system where it regulates root development, including lateral root formation (Reed et al., 357

1998; Bhalerao et al., 2002)(Fig. 3). Interestingly, light signaling affects auxin biosynthesis and 358

transport, implicating this hormone as a potential integrator of light signaling and root 359

development. Phytochrome inactivation in low R:FR light triggers auxin biosynthesis in the shoot 360



16

(Hornitschek et al., 2012), which is then transported laterally through the hypocotyl during low 361

R:FR conditions by PIN3 as well as PIN4 and PIN7 (Keuskamp et al., 2010; Kohnen et al., 2016) 362

and rootward by PIN1 and PIN2 in response to light (Sassi et al., 2012). In darkness, the 363

expression of PIN1 is largely reduced, thus reducing auxin delivery to the root system (Sassi et 364

al., 2012). 365

366

Gibberellic Acid (GA) 367

The plant hormone GA mediates various growth and developmental processes, such as seed 368

germination, cell elongation and reproductive development (Hedden and Sponsel, 2015). Low 369

R:FR induces GA biosynthesis, at least partly through elevated expression of GA20OX genes 370

(Hisamatsu et al., 2005). GAs are diterpenoid tetracyclic carboxylic acids, but only a few are 371

biological active, such as GA1 and GA4 (Hedden and Thomas, 2012). Interestingly, biologically 372

inactive GA12 has been identified as a long-distance growth signal that is transported from the 373

shoot to the root. Here GA12 is converted into active form by GA20ox and GA3ox enzymes and 374

subsequently promotes root growth in Arabidopsis (Regnault et al., 2015)(Fig. 3). It is yet 375

unknown if low R:FR induced production of bioactive GAs in the shoot affects downward GA12 376

transport. 377

378

HY5 379

The transcription factor HY5 is a key integrator of photomorphogenesis and is involved in light, 380

hormone and stress signaling (Cluis et al., 2004; Lee et al., 2007; Gangappa and Botto, 2016). 381

HY5 was recently shown to be transported upon light activation from the shoot to the root (Chen 382

et al., 2016). In the root system, HY5 activates its own expression and that of HY5 383

HOMOLOGUE (HYH), creating a positive feedback loop after shoot-to-root transport of HY5 384

(Zhang et al., 2017). HY5 and HYH modulate lateral root development and lateral root 385

gravitropism (Oyama et al., 1997; Sibout et al., 2006). Interestingly, R:FR ratio’s influence the 386

expression and stability of HY5 and this transcription factor is, therefore, together with auxin and 387

gibberellin a candidate regulator of root developmental adjustments to shoot-sensed R:FR light 388

ratio’s, which indicate the presence of neighboring competitors. 389

390

Functional implications in dense vegetation 391

R:FR light conditions above-ground are a reliable cue for the presence of competing neighbors 392

and effectively trigger shade avoidance (Box 2). Interestingly, if the R:FR ratio signals neighbor 393

proximity, it would also signal the likely presence of neighbors belowground competing for water 394



17

and nutrients (Gundel et al., 2014). Competition experiments in Arabidopsis have shown that 395

root biomass decreases when plants are competing in dense stands and that there is a separate 396

transcriptomic regulation in the root versus the shoot (Masclaux et al., 2012). In controlled 397

growth on medium, seedlings experiencing a low R:FR ratio have a lower lateral root number 398

and main root length (Salisbury et al., 2007). However, as argued previously, in soil conditions 399

the roots are not directly exposed to low R:FR light, and the shoot might thus relay information 400

about nearby competitors to the root system either by direct piping, or through secondary mobile 401

messengers. 402

An important question that remains is what are the functional implications of light signal 403

transmission from the shoot to the root? One clear functional example is that HY5 can stimulate 404

nitrate uptake via NRT2;1, and will do so upon light-activation in the shoot (Chen et al., 405

2016)(Fig. 3). This will help keep the carbon and nitrogen acquisition in tune. In accordance with 406

these findings, direct shading in different phases of the growth period of field-grown maize was 407

shown to suppress root mass, length and absorptive area, suggesting reduced nutrient and/or 408

water uptake rates (Gao et al., 2017). In addition to true shade, a reduced R:FR light ratio also 409

affects root growth in different species (Kasperbauer and Hunt, 1992; Kasperbauer and Hunt, 410

1994; Salisbury et al., 2007). The effects of reduced R:FR ratios on lateral root formation 411

(Salisbury et al, 2007) may go at the expense of nutrient uptake rates, and might reflect a 412

resource prioritization strategy at the whole plant level, ensuring that resources are invested to 413

consolidate light capture in a growing vegetation with increasing competition for light. It is 414

presently unknown if the root architecture responses to low R:FR affect nutrient acquisition at all, 415

but the resulting reduced root length would suggest so. Nevertheless, much more detailed 416

research into nutrient and water uptake rates of plants under high and low R:FR conditions is 417

needed to assess the precise functional implications of shoot-to-root communication of the 418

aboveground light climate. 419

Alternatively, plants may also sense neighbors belowground through for example nutrient 420

depletion zones and chemical exudates. It is unknown if these cues are transferred to the shoot 421

to prepare for upcoming competition or to adjust shoot responses to light cues from neighbors. 422

Finally, abiotic stresses, e.g. drought, occur primarily in the belowground environment and may 423

interact with aboveground light responses. Although little is known about interactions between 424

abiotic stresses and shade responses of the shoot, there is ample information about the 425

interaction of biotic stress and neighbor detection through light cues. The emerging picture is 426

that shade avoidance responses and phytochrome signaling dominate plant defenses against 427

pathogenic microorganisms and against insects (De Wit et al., 2013; Ballaré, 2014), thus 428



18

prioritizing light interception. It will be interesting to study if next to biotic stresses, responses 429

against abiotic stresses are suppressed to accommodate shade avoidance responses at high 430

plant density. 431

432

433

Concluding remarks 434

Plants have a variety of photoreceptors that control many different aspects of plant life, including 435

root development. Recently, several novel mechanisms have been discovered that allow plants 436

to relay information from the shoot and its environment to the root system. These include direct 437

light transmission, hormones and mobile proteins. Although research into these different 438

mechanisms will continue to identify novel mechanisms, it is also crucial to establish the 439

functional implications of this information transfer. It is therefore, pertinent that ecologists, 440

agronomists and plant scientists join forces to unravel both the mechanisms and functional 441

implications of shoot-root communication induced by light cues from the environment. 442

443

444

445



19

Figure Legends 446

447

Figure 1. Relative amounts of photoreceptors in Arabidopsis tissues. 448

The graph displays the relative expression of photoreceptors across seedling tissues. Both gene 449

expression and protein (when data are available) abundance are shown. The box that groups 450

classes of receptors indicates that intensities within can be compared. In the phytochrome box 451

‘L’ stands for protein levels in light and ‘D’ for protein levels in the dark. Source data: For all, 452

BAR eFP browser (http://bar.utoronto.ca/efp/cgi-bin/efpWeb.cgi), phytochromes (Somers and 453

Quail, 1995; Goosey et al., 1997; Toth et al., 2001; Sharrock and Clack, 2002; Salisbury et al., 454

2007), phototropins (Sakamoto and Briggs, 2002; Moni et al., 2015), cryptochromes (Toth et al., 455

2001), and UVR8 (Rizzini et al., 2011). 456

457

Figure 2. Root growth is affected by light quantity and quality. 458

(A) 8d old seedlings grown on ½ MS medium in darkness and white light (WL) (140µM m-2 s-1 459

photosynthetically active radiation, PAR). (B) 8d old seedling grown in WL (140µM m-2 s-1 ) or 460

WL+FR (R:FR 0.1). The arrows point to the root-shoot junctions. 461

462

Figure 3. The aboveground regulation of root development in dense vegetation involves 463

photosynthesis, light piping, hormones and mobile factors. 464

The primary effect of light is to enable photosynthesis which leads to the production of sugars 465

(sucrose), that enable the root to grow. Photomorphogenic development is associated with the 466

production of auxins in the shoot, which are transported rootward and enable root development. 467

HY5 is stabilized in the shoot during photomorphogenesis and is transported rootwards where it 468

regulates nitrate uptake and root development. 469

Light is used as a cue to detect neighboring plant competition via sensing of the R:FR ratio. 470

Plant tissues reflect FR, which lowers the nearby R:FR ratio, leading to shade avoidance 471

responses mediated by, amongst others, auxin and GA. These hormones can be transported 472

rootward where they affect root development. There are also indications that shade avoidance 473

responses, in a negative feedback mechanism, decrease the amount of rootward auxin 474

transport. FR light itself can also be transmitted directly through woody, vascular, tissues from 475

the shoot to the root, where it can affect root-localized phytochromes. 476

477

478

479



20

Box 2 Figure. Shade avoidance induced by low R:FR. Carrot (Daucus carota) plants grown in white light 480

(WL; left) and WL+FR (right). Plants were grown in WL or WL+FR for 8 weeks. PAR was ~120 μmol 481

m−2 s−1, and the FR ratio was 1.8 (WL and 0.2 (WL+FR). Scale bar = 1 cm. 482

483



21

484



WL WL+FR

BOX2, Figure A. Shade avoidance induced by low R:FR.

Carrot (Daucus carota) plants grown in white light (WL; left) and WL +FR (right). Plants were grown in WL or WL +FR for 8 weeks. PAR was --120 µmol m-2 s-1

, and the FR ratio was 1.8 (WL and 0.2 (WL +FR). Scale bar = 1 cm. www.plantphysiol.orgon August 27, 2018 - Published by Downloaded from

Copyright © 2017 American Society of Plant Biologists. All rights reserved.


ADVANCES

• New modes of information transfer between the

shoot and root stems have been identified,

including light piping and the light-sensitive

transcription factor HY5.

• Light signaling interacts with root-environment

interactions, including nutrient acquisition and

gravitropism.

• A vertical agar plate system for Arabidopsis

growth, D-root, was developed to keep roots in

darkness, while the shoot experiences light. This

system has allowed probing direct and indirect

light effects on root system architecture.



OUTSTANDING QUESTIONS

• Do plants use light cues associated with density

in vegetation to adjust root development,

architecture, and nutrient acquisition physiology

to neighbors?

• Do root responses to soil (stress) conditions

affect aboveground (architectural) responses to

light signals?

• Which mobile signals control root system

architecture upon photoreceptor activation by

different wavebands in the shoot, and through

which tissue(s) do these factors travel towards

the root system?

• Is there strong genetic variation for light (quality

and quantity) effects on root development, or

are these broadly occurring responses

throughout the higher plant kingdom?



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Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2012) SCF(TIR1/AFB)-auxinsignalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32: 260–274


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http://www.ncbi.nlm.nih.gov/pubmed?term=De Rybel B%2C Vassileva V%2C Parizot B%2C Demeulenaere M%2C Grunewald W%2C Audenaert D%2C Van Campenhout J%2C Overvoorde P%2C Jansen L%2C Vanneste S%2C et al %282010%29 A novel aux%2FIAA28 signaling cascade activates GATA23%2Ddependent specification of lateral root founder cell identity%2E Curr Biol 20%3A 1697�??706&dopt=abstract

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Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130:442–56


Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof Y-D, Huq E, Hiltbrunner A (2015)Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis byreorganizing the COP1/SPA complex. Plant Cell 27: 189–201


Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS (2006) Opposite root growth phenotypes of hy5 versus hy5 hyhmutants correlate with increased constitutive auxin signaling. PLoS Genet 2: e202


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Silva-Navas J, Moreno-Risueno MA, Manzano C, Téllez-Robledo B, Navarro-Neila S, Carrasco V, Pollmann S, Gallego FJ, del Pozo JC(2016) Flavonols Mediate Root Phototropism and Growth through Regulation of Proliferation-to-Differentiation Transition. Plant Cell28: 1372–1387


De Smet I, Tetsumura T, De Rybel B, Frey NF d., Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, et al (2007)Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681–690


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Pubmed: Author and Title www.plantphysiol.orgon August 27, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Seo HS%2C Yang J%2DY%2C Ishikawa M%2C Bolle C%2C Ballesteros ML%2C Chua N%2DH %282003%29 LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1%2E Nature 423%3A 995�??999&dopt=abstract

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

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http://search.crossref.org/?page=1&rows=2&q=Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130: 442?56

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http://scholar.google.com/scholar?as_q=Patterns of expression and normalized levels of the five Arabidopsis phytochromes.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Sheerin DJ%2C Menon C%2C zur Oven%2DKrockhaus S%2C Enderle B%2C Zhu L%2C Johnen P%2C Schleifenbaum F%2C Stierhof Y%2DD%2C Huq E%2C Hiltbrunner A %282015%29 Light%2Dactivated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1%2FSPA complex%2E Plant Cell 27%3A 189�??201&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof Y-D, Huq E, Hiltbrunner A (2015) Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. Plant Cell 27: 189?201

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

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http://scholar.google.com/scholar?as_q=Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sheerin&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sibout R%2C Sukumar P%2C Hettiarachchi C%2C Holm M%2C Muday GK%2C Hardtke CS %282006%29 Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling%2E PLoS Genet 2%3A e202&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS (2006) Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genet 2: e202

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

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http://scholar.google.com/scholar?as_q=Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sibout&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Silva%2DNavas J%2C Moreno%2DRisueno MA%2C Manzano C%2C Pallero%2DBaena M%2C Navarro%2DNeila S%2C Tellez%2DRobledo B%2C Garcia%2DMina JM%2C Baigorri R%2C Gallego FJ%2C Del Pozo JC %282015%29 D%2DRoot%3A A system for cultivating plants with the roots in darkness or under different light conditions%2E Plant J 84%3A 244�??255&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Silva-Navas J, Moreno-Risueno MA, Manzano C, Pallero-Baena M, Navarro-Neila S, Tellez-Robledo B, Garcia-Mina JM, Baigorri R, Gallego FJ, Del Pozo JC (2015) D-Root: A system for cultivating plants with the roots in darkness or under different light conditions. Plant J 84: 244?255

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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Silva%2DNavas J%2C Moreno%2DRisueno MA%2C Manzano C%2C Téllez%2DRobledo B%2C Navarro%2DNeila S%2C Carrasco V%2C Pollmann S%2C Gallego FJ%2C del Pozo JC %282016%29 Flavonols Mediate Root Phototropism and Growth through Regulation of Proliferation%2Dto%2DDifferentiation Transition%2E Plant Cell 28%3A 1372�??1387&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Smith H %281982%29 Light Quality%2C Photoperception%2C and Plant Strategy%2E Annu Rev Plant Physiol 481�??518&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Smith H (1982) Light Quality, Photoperception, and Plant Strategy. Annu Rev Plant Physiol 481?518

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http://scholar.google.com/scholar?as_q=Light Quality, Photoperception, and Plant Strategy.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Smith&as_ylo=1982&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Somers DE%2C Quail PH %281995%29 Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis%2E Plant J 7%3A 413�??427&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Somers DE, Quail PH (1995) Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis. Plant J 7: 413?427

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http://scholar.google.com/scholar?as_q=Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Stepanova AN%2C Robertson%2DHoyt J%2C Yun J%2C Benavente LM%2C Xie D%2DY%2C Dolezal K%2C Schlereth A%2C Jürgens G%2C Alonso JM %282008%29 TAA1%2Dmediated auxin biosynthesis is essential for hormone crosstalk and plant development%2E Cell 133%3A 177�??91&dopt=abstract

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Suzuki H, Yokawa K, Nakano S, Yoshida Y, Fabrissin I, Okamoto T, Baluska F, Koshiba T (2016) Root cap-dependent gravitropic U-turnof maize root requires light-induced auxin biosynthesis via the YUC pathway in the root apex. J Exp Bot 67: 4581–4591


Sweere U (2001) Interaction of the Response Regulator ARR4 with Phytochrome B in Modulating Red Light Signaling. Science (80- )294: 1108–1111


Tong H, Leasure CD, Hou X, Yuen G, Briggs W, He Z-H (2008) Role of root UV-B sensing in Arabidopsis early seedling development.Proc Natl Acad Sci U S A 105: 21039–44


Toth R, Kevei E, Hall A, Millar AJ, Nagy F, Kozma-Bognar L (2001) Circadian Clock-Regulated Expression of Phytochrome andCryptochrome Genes in Arabidopsis. Plant Physiol 127: 1607–1616


Vermeer JEM, von Wangenheim D, Barberon M, Lee Y, Stelzer EHK, Maizel A, Geldner N (2014) A spatial accommodation byneighboring cells is required for organ initiation in Arabidopsis. Science 343: 178–83


Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluska F, Lin J (2012) The Signal Transducer NPH3 Integrates thePhototropin1 Photosensor with PIN2-Based Polar Auxin Transport in Arabidopsis Root Phototropism. Plant Cell 24: 551–565


Weiner J (1985) Size hierarchies in experimental populations of annual plants. Ecology 66: 743–752Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Weiner J, Thomas SC (1986) Size variability and competition in plant monocultures. Oikos 47: 211–222Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

de Wit M, Keuskamp DH, Bongers FJ, Hornitschek P, Gommers CMM, Reinen E, Martinez-Ceron C, Fankhauser C, Pierik R (2016)Integration of Phytochrome and Cryptochrome Signals Determines Plant Growth during Competition for Light. Curr Biol 26: 3320–3326


De Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ, Voesenek L a CJ, Pierik R (2013) Perception of low red: Far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J 75: 90–103


Wu S-H (2014) Gene expression regulation in photomorphogenesis from the perspective of the central dogma. Annu Rev Plant Biol 65:311–33


Xu W, Ding G, Yokawa K, Baluška F, Li Q-F, Liu Y, Shi W, Liang J, Zhang J (2013) An improved agar-plate method for studying rootgrowth and response of Arabidopsis thaliana. Sci Rep 3: 1273


Xu X, Paik I, Zhu L, Huq E (2015) Illuminating Progress in Phytochrome-Mediated Light Signaling Pathways. Trends Plant Sci 20: 641–650

Pubmed: Author and Title www.plantphysiol.orgon August 27, 2018 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

http://search.crossref.org/?page=1&rows=2&q=Sun Q, Yoda K, Suzuki M, Suzuki H (2003) Vascular tissue in the stem and roots of woody plants can conduct light. J Exp Bot 54: 1627?1635

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http://search.crossref.org/?page=1&rows=2&q=Suzuki H, Yokawa K, Nakano S, Yoshida Y, Fabrissin I, Okamoto T, Baluska F, Koshiba T (2016) Root cap-dependent gravitropic U-turn of maize root requires light-induced auxin biosynthesis via the YUC pathway in the root apex. J Exp Bot 67: 4581?4591

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http://search.crossref.org/?page=1&rows=2&q=Sweere U (2001) Interaction of the Response Regulator ARR4 with Phytochrome B in Modulating Red Light Signaling. Science (80- ) 294: 1108?1111

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http://search.crossref.org/?page=1&rows=2&q=Tong H, Leasure CD, Hou X, Yuen G, Briggs W, He Z-H (2008) Role of root UV-B sensing in Arabidopsis early seedling development. Proc Natl Acad Sci U S A 105: 21039?44

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http://www.ncbi.nlm.nih.gov/pubmed?term=Xu X%2C Paik I%2C Zhu L%2C Huq E %282015%29 Illuminating Progress in Phytochrome%2DMediated Light Signaling Pathways%2E Trends Plant Sci 20%3A 641�??650&dopt=abstract


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http://search.crossref.org/?page=1&rows=2&q=Xu X, Paik I, Zhu L, Huq E (2015) Illuminating Progress in Phytochrome-Mediated Light Signaling Pathways. Trends Plant Sci 20: 641?650

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Light signaling, root development and plasticity · 2 Light signaling, root development and...

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