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Molecular Regulation of Plant Responses to Shade

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Progress in Botany Vol. 84

Part of the book series: Progress in Botany ((BOTANY,volume 84))

Abstract

In sun-loving plants, detection of the proximity of nearby competitors triggers a set of responses known as the shade-avoidance syndrome (SAS). These responses will help the plant to acclimate to the proximity of vegetation that might compromise light availability and limit plant development. Plants sense the presence of nearby competitor vegetation as changes in the light quality, i.e. a reduced red (R) to far-red light (FR) ratio (R:FR). Among the various responses to neighboring plants, one of the best studied and characterized is the promotion of the hypocotyl elongation in seedlings of the model plant Arabidopsis thaliana that might help them to outcompete neighboring seedlings and reach better light conditions. In addition to this and other developmental changes, shade perception affects photosynthetic capacity and reduces plant defense. In this chapter, we will review the main molecular aspects that control the regulation of hypocotyl elongation, including the role of the phytochrome photoreceptors, that sense the signal, and the best known genetic and hormonal components that participate downstream shade perception. Because of the obvious interest for translating this knowledge to agriculture, we will also explore what is known about the molecular interaction between shade perception, defense responses, and the growth-defense trade-off observed in high planting density.

Communicated by Francisco M. Cánovas

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References

  • Ballare CL (2009) Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ 32:713–725

    PubMed  Google Scholar 

  • Ballare CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363

    PubMed  Google Scholar 

  • Ballare CL, Austin AT (2019) Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates. J Exp Bot 70:3425–3434

    PubMed  Google Scholar 

  • Ballare CL, Pierik R (2017) The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ 40:2530–2543

    PubMed  Google Scholar 

  • Bou-Torrent J, Roig-Villanova I, Martinez-Garcia JF (2008) Light signaling: back to space. Trends Plant Sci 13:108–114

    PubMed  Google Scholar 

  • Bou-Torrent J, Galstyan A, Gallemi M, Cifuentes-Esquivel N, Molina-Contreras MJ, Salla-Martret M, Jikumaru Y, Yamaguchi S, Kamiya Y, Martinez-Garcia JF (2014) Plant proximity perception dynamically modulates hormone levels and sensitivity in Arabidopsis. J Exp Bot 65:2937–2947

    PubMed  PubMed Central  Google Scholar 

  • Bou-Torrent J, Toledo-Ortiz G, Ortiz-Alcaide M, Cifuentes-Esquivel N, Halliday KJ, Martinez-Garcia JF, Rodriguez-Concepcion M (2015) Regulation of carotenoid biosynthesis by shade relies on specific subsets of antagonistic transcription factors and cofactors. Plant Physiol 169:1584–1594

    PubMed  PubMed Central  Google Scholar 

  • Brandt R, Salla-Martret M, Bou-Torrent J, Musielak T, Stahl M, Lanz C, Ott F, Schmid M, Greb T, Schwarz M, Choi SB, Barton MK, Reinhart BJ, Liu T, Quint M, Palauqui JC, Martinez-Garcia JF, Wenkel S (2012) Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J 72:31–42

    PubMed  Google Scholar 

  • Casal JJ (2012) Shade avoidance. In: Arabidopsis book, vol 10, p e0157

    Google Scholar 

  • Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol 64:403–427

    PubMed  Google Scholar 

  • Chico JM, Fernandez-Barbero G, Chini A, Fernandez-Calvo P, Diez-Diaz M, Solano R (2014) Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 26:1967–1980

    PubMed  PubMed Central  Google Scholar 

  • Cifuentes-Esquivel N, Bou-Torrent J, Galstyan A, Gallemi M, Sessa G, Salla Martret M, Roig-Villanova I, Ruberti I, Martinez-Garcia JF (2013) The bHLH proteins BEE and BIM positively modulate the shade avoidance syndrome in Arabidopsis seedlings. Plant J 75:989–1002

    PubMed  Google Scholar 

  • Ciolfi A, Sessa G, Sassi M, Possenti M, Salvucci S, Carabelli M, Morelli G, Ruberti I (2013) Dynamics of the shade-avoidance response in Arabidopsis. Plant Physiol 163:331–353

    PubMed  PubMed Central  Google Scholar 

  • Crocco CD, Holm M, Yanovsky MJ, Botto JF (2010) AtBBX21 and COP1 genetically interact in the regulation of shade avoidance. Plant J 64:551–562

    PubMed  Google Scholar 

  • Datta S, Johansson H, Hettiarachchi C, Irigoyen ML, Desai M, Rubio V, Holm M (2008) LZF1/SALT TOLERANCE HOMOLOG3, an Arabidopsis B-box protein involved in light-dependent development and gene expression, undergoes COP1-mediated ubiquitination. Plant Cell 20:2324–2338

    PubMed  PubMed Central  Google Scholar 

  • De Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ, Voesenek L, 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

    PubMed  Google Scholar 

  • Djakovic-Petrovic T, De Wit M, Voesenek LA, Pierik R (2007) DELLA protein function in growth responses to canopy signals. Plant J 51:117–126

    PubMed  Google Scholar 

  • Fankhauser C, Casal JJ (2004) Phenotypic characterization of a photomorphogenic mutant. Plant J 39:747–760

    PubMed  Google Scholar 

  • Fernandez-Milmanda GL, Ballare CL (2021) Shade avoidance: expanding the color and hormone palette. Trends Plant Sci 26:509–523

    PubMed  Google Scholar 

  • Fernandez-Milmanda GL, Crocco CD, Reichelt M, Mazza CA, Kollner TG, Zhang T, Cargnel MD, Lichy MZ, Fiorucci AS, Fankhauser C, Koo AJ, Austin AT, Gershenzon J, Ballare CL (2020) A light-dependent molecular link between competition cues and defence responses in plants. Nat Plants 6:223–230

    PubMed  Google Scholar 

  • Fiorucci AS, Fankhauser C (2017) Plant strategies for enhancing access to sunlight. Curr Biol 27:R931–R940

    PubMed  Google Scholar 

  • Gallemi M, Molina-Contreras MJ, Paulisic S, Salla-Martret M, Sorin C, Godoy M, Franco-Zorrilla JM, Solano R, Martinez-Garcia JF (2017) A non-DNA-binding activity for the ATHB4 transcription factor in the control of vegetation proximity. New Phytol 216:798–813

    PubMed  Google Scholar 

  • Ganesan M, Lee HY, Kim JI, Song PS (2017) Development of transgenic crops based on photo-biotechnology. Plant Cell Environ 40:2469–2486

    PubMed  Google Scholar 

  • Gangappa SN, Crocco CD, Johansson H, Datta S, Hettiarachchi C, Holm M, Botto JF (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25:1243–1257

    PubMed  PubMed Central  Google Scholar 

  • Gommers CM, Visser EJ, St Onge KR, Voesenek LA, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends Plant Sci 18:65–71

    PubMed  Google Scholar 

  • Gommers CM, Keuskamp DH, Buti S, Van Veen H, Koevoets IT, Reinen E, Voesenek LA, Pierik R (2017) Molecular profiles of contrasting shade response strategies in wild plants: differential control of immunity and shoot elongation. Plant Cell 29:331–344

    PubMed  PubMed Central  Google Scholar 

  • Hayes S, Velanis CN, Jenkins GI, Franklin KA (2014) UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance. Proc Natl Acad Sci U S A 111:11894–11899

    PubMed  PubMed Central  Google Scholar 

  • Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28:3893–3902

    PubMed  PubMed Central  Google Scholar 

  • Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711

    PubMed  Google Scholar 

  • Jeong J, Choi G (2013) Phytochrome-interacting factors have both shared and distinct biological roles. Mol Cells 35:371–380

    PubMed  PubMed Central  Google Scholar 

  • Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis (phytochrome A is required for the perception of daylength extensions). Plant Physiol 105:141–149

    PubMed  PubMed Central  Google Scholar 

  • Keuskamp DH, Pollmann S, Voesenek LA, Peeters AJ, Pierik R (2010) Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc Natl Acad Sci U S A 107:22740–22744

    PubMed  PubMed Central  Google Scholar 

  • Kohnen MV, Schmid-Siegert E, Trevisan M, Petrolati LA, Senechal F, Muller-Moule P, Maloof J, Xenarios I, Fankhauser C (2016) Neighbor detection induces organ-specific transcriptomes, revealing patterns underlying hypocotyl-specific growth. Plant Cell 28:2889–2904

    PubMed  PubMed Central  Google Scholar 

  • Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16:19–28

    PubMed  Google Scholar 

  • Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, Quail PH (2012) Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24:1398–1419

    PubMed  PubMed Central  Google Scholar 

  • Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung HS, Ecker JR, Kay SA, Chory J (2012) Linking photoreceptor excitation to changes in plant architecture. Genes Dev 26:785–790

    PubMed  PubMed Central  Google Scholar 

  • Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53:312–323

    PubMed  Google Scholar 

  • Martinez-Garcia JF, Santes CM, Garcia-Martinez JL (2000) The end-of-day far-red irradiation increases gibberellin A1 content in cowpea (Vigna sinensis L.) by reducing its inactivation. Physiol Plant 108:426–434

    Google Scholar 

  • Martinez-Garcia JF, Galstyan A, Salla-Martret M, Cifuentes-Esquivel N, Gallemí M, Bou-Torrent J (2010) Regulatory components of shade avoidance syndrome. Adv Bot Res 53:65–116

    Google Scholar 

  • Martinez-Garcia JF, Gallemi M, Molina-Contreras MJ, Llorente B, Bevilaqua MR, Quail PH (2014) The shade avoidance syndrome in Arabidopsis: the antagonistic role of phytochrome a and B differentiates vegetation proximity and canopy shade. PLoS One 9:e109275

    PubMed  PubMed Central  Google Scholar 

  • Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, Mcsteen P, Zhao Y, Hayashi K, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci U S A 108:18512–18517

    PubMed  PubMed Central  Google Scholar 

  • Mcnellis TW, Von Arnim AG, Araki T, Komeda Y, Misera S, Deng XW (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6:487–500

    PubMed  PubMed Central  Google Scholar 

  • Molina-Contreras MJ, Paulisic S, Then C, Moreno-Romero J, Pastor-Andreu P, Morelli L, Roig-Villanova I, Jenkins H, Hallab A, Gan X, Gomez-Cadenas A, Tsiantis M, Rodriguez-Concepcion M, Martinez-Garcia JF (2019) Photoreceptor activity contributes to contrasting responses to shade in cardamine and Arabidopsis seedlings. Plant Cell 31:2649–2663

    PubMed  PubMed Central  Google Scholar 

  • Morelli L, Paulisic S, Qin W, Iglesias-Sanchez A, Roig-Villanova I, Florez-Sarasa I, Rodriguez-Concepcion M, Martinez-Garcia JF (2021) Light signals generated by vegetation shade facilitate acclimation to low light in shade-avoider plants. Plant Physiol 186:2137–2151

    PubMed  PubMed Central  Google Scholar 

  • Moreno JE, Tao Y, Chory J, Ballare CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci U S A 106:4935–4940

    PubMed  PubMed Central  Google Scholar 

  • Nito K, Kajiyama T, Unten-Kobayashi J, Fujii A, Mochizuki N, Kambara H, Nagatani A (2015) Spatial regulation of the gene expression response to shade in Arabidopsis seedlings. Plant Cell Physiol 56:1306–1319

    PubMed  Google Scholar 

  • Ortiz-Alcaide M, Llamas E, Gomez-Cadenas A, Nagatani A, Martinez-Garcia JF, Rodriguez-Concepcion M (2019) Chloroplasts modulate elongation responses to canopy shade by retrograde pathways involving HY5 and ABA. Plant Cell

    Google Scholar 

  • Pacin M, Legris M, Casal JJ (2013) COP1 re-accumulates in the nucleus under shade. Plant J 75:631–641

    PubMed  Google Scholar 

  • Pacin M, Semmoloni M, Legris M, Finlayson SA, Casal JJ (2016) Convergence of constitutive photomorphogenesis 1 and phytochrome interacting factor signalling during shade avoidance. New Phytol 211:967–979

    PubMed  Google Scholar 

  • Pierik R, Ballare CL (2021) Control of plant growth and defense by photoreceptors: from mechanisms to opportunities in agriculture. Mol Plant 14:61–76

    PubMed  Google Scholar 

  • Pierik R, Testerink C (2014) The art of being flexible: how to escape from shade, salt, and drought. Plant Physiol 166:5–22

    PubMed  PubMed Central  Google Scholar 

  • Possart A, Fleck C, Hiltbrunner A (2014) Shedding (far-red) light on phytochrome mechanisms and responses in land plants. Plant Sci 217–218:36–46

    PubMed  Google Scholar 

  • Procko C, Crenshaw CM, Ljung K, Noel JP, Chory J (2014) Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa. Plant Physiol 165:1285–1301

    PubMed  PubMed Central  Google Scholar 

  • Roig-Villanova I, Martinez-Garcia JF (2016) Plant responses to vegetation proximity: a whole life avoiding shade. Front Plant Sci 7:236

    PubMed  PubMed Central  Google Scholar 

  • Roig-Villanova I, Bou J, Sorin C, Devlin PF, Martinez-Garcia JF (2006) Identification of primary target genes of phytochrome signaling. Early transcriptional control during shade avoidance responses in Arabidopsis. Plant Physiol 141:85–96

    PubMed  PubMed Central  Google Scholar 

  • Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Concepcion M, Martinez-Garcia JF (2007) Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO J 26:4756–4767

    PubMed  PubMed Central  Google Scholar 

  • Roig-Villanova I, Paulisic S, Martinez-Garcia JF (2019) Shade avoidance and neighbor detection. Methods Mol Biol 2026:157–168

    PubMed  Google Scholar 

  • Salter MG, Franklin KA, Whitelam GC (2003) Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426:680–683

    PubMed  Google Scholar 

  • Sellaro R, Yanovsky MJ, Casal JJ (2011) Repression of shade-avoidance reactions by sunfleck induction of HY5 expression in Arabidopsis. Plant J 68:919–928

    PubMed  Google Scholar 

  • Sessa G, Carabelli M, Sassi M, Ciolfi A, Possenti M, Mittempergher F, Becker J, Morelli G, Ruberti I (2005) A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev 19:2811–2815

    PubMed  PubMed Central  Google Scholar 

  • Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33:481–518

    Google Scholar 

  • Smith H (2000) Phytochromes and light signal perception by plants – an emerging synthesis. Nature 407:585–591

    PubMed  Google Scholar 

  • Song B, Zhao H, Dong K, Wang M, Wu S, Li S, Wang Y, Chen P, Jiang L, Tao Y (2020) Phytochrome A inhibits shade avoidance responses under strong shade through repressing the brassinosteroid pathway in Arabidopsis. Plant J 104:1520–1534

    PubMed  Google Scholar 

  • Sorin C, Salla-Martret M, Bou-Torrent J, Roig-Villanova I, Martinez-Garcia JF (2009) ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant J 59:266–277

    PubMed  Google Scholar 

  • Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    PubMed  PubMed Central  Google Scholar 

  • Van Gelderen K, Kang C, Paalman R, Keuskamp D, Hayes S, Pierik R (2018) Far-red light detection in the shoot regulates lateral root development through the HY5 transcription factor. Plant Cell 30:101–116

    PubMed  PubMed Central  Google Scholar 

  • Yang C, Li L (2017) Hormonal regulation in shade avoidance. Front Plant Sci 8:1527

    PubMed  PubMed Central  Google Scholar 

  • Yang C, Xie F, Jiang Y, Li Z, Huang X, Li L (2018) Phytochrome A negatively regulates the shade avoidance response by increasing auxin/indole acidic acid protein stability. Dev Cell 44(29-41):e24

    Google Scholar 

  • Zhao Y (2014) Auxin biosynthesis. In: Arabidopsis book, vol 12, p e0173

    Google Scholar 

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Acknowledgments

The authors are supported by grant PID2020-115782GB-I00 from Spanish MCIN/AEI (10.13039/501100011033), by the EU PRIMA project UToPIQ (MCIN/AEI code PCI2021-121941), the Generalitat Valenciana project ENIGmA (PROMETEU/2021/056), and the Consejo Superior de Investigaciones Cientificas (CSIC code 202040E256).

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Correspondence to Jaime F. Martinez-Garcia .

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Roig-Villanova, I., Martinez-Garcia, J.F. (2022). Molecular Regulation of Plant Responses to Shade. In: Lüttge, U., Cánovas, F.M., Risueño, MC., Leuschner, C., Pretzsch, H. (eds) Progress in Botany Vol. 84. Progress in Botany, vol 84. Springer, Cham. https://doi.org/10.1007/124_2022_66

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