Abstract
In the late nineteenth century, Charles Darwin observed that ‘light exerts a powerful influence on most vegetable tissues, and there can be no doubt that it generally tends to check their growth’ (The Power of Movement in Plants, 1880). Subsequent to this seminal work, light has been recognised as an important regulator of plant growth. Over the next 150 years, research on light regulation of plant growth and development by immensely imaginative and talented researchers in various laboratories across the globe has given us tremendous insights into how light governs plant growth both at the organismal and molecular levels. The discovery of light-responsive photoreceptor proteins that are activated by red, far-red, blue/UV-A and UV-B light has helped further our understanding of how plants respond to the light that falls on the surface of the earth. This chapter brings together the recent developments in our understanding of how plants sense light by using photoreceptors and the various molecular mechanisms involved in light perception and transmission of the light signal within the plant. Furthermore, the chapter discusses recently ascribed functions of photoreceptors such as the ability of plants to distinguish their kin from non-kin through the action of phytochrome, the role(s) of cryptochrome as a magnetoreceptor and the role of phytochrome and phototropin as temperature sensors. The chapter also rekindles the debate about whether plants can have vision despite the lack of optical or light-sensitive organs such as eyes.
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Ahmad M, Galland P, Ritz T, Wiltschko R, Wiltschko W (2007) Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225:615–624
Al-Sady B, Ni W, Kircher S, Schäfer E, Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23:439–446
Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639
Baluška F, Mancuso S (2016) Vision in plants via plant-specific ocelli? Trends Plant Sci 21:727–730
Banerjee R, Schleicher E, Meier S, Viana RM, Pokorny R, Ahmad M et al (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J Biol Chem 282:14916–14922
Bauer D, Viczián AS, Kircher S, Nobis T, Nitschke R, Kunkel T et al (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3: a transcription factor required for light signaling in Arabidopsis. Plant Cell 16:1433–1445
Bouly J, Schleicher E, Dionisio-Sese M, Vandenbussche F, Van Der Straeten D, Bakrim N et al (2007) Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J Biol Chem 282:9383–9391
Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210
Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD (2014) Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proc Natl Acad Sci U S A 111:10179–10184
Chen M, Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21:664–671
Chen X, Yao Q, Gao X, Jiang C, Harberd Nicholas P, Fu X (2016) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr Biol 26:640–646
Cho HY, Tseng TS, Kaiserli E, Sullivan S, Christie JM, Briggs WR (2007) Physiological roles of the light, oxygen, or voltage domains of phototropin 1 and phototropin 2 in Arabidopsis. Plant Physiol 143:517–529
Christie JM, Salomon M, Nozue K, Wada M, Briggs WR (1999) LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci U S A 96:8779–8783
Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J et al (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9:e1001076
Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A et al (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–1496
Christie JM, Blackwood L, Petersen J, Sullivan S (2015) Plant flavoprotein photoreceptors. Plant Cell Physiol 56:401–413
Crepy MA, Casal JJ (2015) Photoreceptor-mediated kin recognition in plants. New Phytol 205:329–338
Demarsy E, Schepens I, Okajima K, Hersch M, Bergmann S, Christie JM et al (2012) Phytochrome Kinase Substrate 4 is phosphorylated by the phototropin 1 photoreceptor. EMBO J 31:3457–3467
Demkura PV, Ballaré CL (2012) UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol Plant 5:642–652
Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133:1617–1629
Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438
Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M et al (2009) Interaction of COP1 and UVR8 regulates UV-B induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28:591–601
Franklin KA (2008) Shade avoidance. New Phytol 179:930–944
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C et al (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci U S A 108:20231–20235
Fujii Y, Tanaka H, Konno N, Ogasawara Y, Hamashima N, Tamura S et al (2017) Phototropin perceives temperature based on the lifetime of its photoactivated state. Proc Natl Acad Sci U S A 114:9206–9211
Gianoli E (2017) Eyes in the chameleon vine? Trends Plant Sci 22:4–5
Gianoli E, Carrasco-Urra F (2014) Leaf mimicry in a climbing plant protects against herbivory. Curr Biol 24:984–987
Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat Struct Mol Biol 10:489–490
Goyal A, Karayekov E, Galvão VC, Ren H, Casal JJ, Fankhauser C (2016) Shade promotes phototropism through phytochrome B-controlled auxin production. Curr Biol 26:3280–3287
Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot 103:1165–1172
Gupta SK, Sharma S, Santisree P, Kilambi HV, Appenroth K, Sreelakshmi Y et al (2014) Complex and shifting interactions of phytochromes regulate fruit development in tomato. Plant Cell Environ 37:1688–1702
Haberlandt G (1905) Die Lichtsinnesorgane der Laubblätter. W. Engelmann, Leipzig
Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25
Hohm T, Demarsy E, Quan CM, Petrolati LA, Preuten T, Vernoux T et al (2014) Plasma membrane H+-ATPase regulation is required for auxin gradient formation preceding phototropic growth. Mol Syst Biol 10:751
Huang X, Ouyang X, Yang P, Lau OS, Li G, Li J et al (2012) Arabidopsis FHY3 and HY5 positively mediate induction of COP1 transcription in response to photomorphogenic UV-B light. Plant Cell 24:4590–4606
Huang X, Yang P, Ouyang X, Chen L, Deng XW (2014) Photoactivated UVR8-COP1 module determines photomorphogenic UV-B signaling output in Arabidopsis. PLoS Genet 10:e1004218
Inoue S, Kinoshita T (2008) Blue light regulation of stomatal opening and the plasma membrane H+-ATPase. Plant Physiol 174:531–538
Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582
Itoh H, Nonoue Y, Yano M, Izawa T (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat Genet 42:635
Iwabuchi K, Minamino R, Takagi S (2010) Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis leaf cells. Plant Physiol 152:1309–1319
Jones MA, Feeney KA, Kelly SM, Christie JM (2007) Mutational analysis of phototropin 1 provides insights into the mechanism underlying LOV2 signal transmission. J Biol Chem 282(9):6405–6414
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T et al (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141
Kasahara M, Torii M, Fujita A, Tainaka K (2010) FMN binding and photochemical properties of plant putative photoreceptors containing two LOV domains, LOV/LOV proteins. J Biol Chem 285:34765–34772
Kircher S, Schopfer P (2012) Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc Natl Acad Sci U S A 109:11217–11221
Lee H, Ha J, Kim S, Choi H, Kim Z, Han Y et al (2016) Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Sci Signal 9:ra106
Lee B, Kim MR, Kang M, Cha J, Han S, Nawkar GM et al (2017) The F-box protein FKF1 inhibits dimerization of COP1 in the control of photoperiodic flowering. Nat Commun 8:2259
Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hiltbrunner A et al (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354:897–900
Legris M, Nieto C, Sellaro R, Prat S, Casal JJ (2017) Perception and signalling of light and temperature cues in plants. Plant J 90:683–697
Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26:56–78
Leivar P, Monte E, Al-Sady B, Carle C, Storer A, Alonso JM et al (2008) The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20:337–352
Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272:398–401
Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. The Arabidopsis Book, American Society for Plant Biologists, Rockville
Lian H, He S, Zhang Y, Zhu D, Zhang J, Jia K et al (2011) Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev 25:1023–1028
Liedvogel M, Mouritsen H (2010) Cryptochrome-a potential magnetoreceptor: what do we know and what do we want to know? J R Soc Interface 7:S147–S162
Lin C, Robertson DE, Ahmad M, Raibekas AA, Jorns MS, Dutton PL et al (1995) Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1. Science 269:968–970
Liu H, Wang Q, Liu Y, Zhao X, Imaizumi T, Somers DE et al (2013) Arabidopsis CRY2 and ZTL mediate blue-light regulation of the transcription factor CIB1 by distinct mechanisms. Proc Natl Acad Sci U S A 110:17582–17587
Maeda K, Robinson AJ, Henbest KB, Hogben HJ, Biskup T, Ahmad M et al (2012) Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proc Natl Acad Sci U S A 109:4774–4779
Maffei ME (2014) Magnetic field effects on plant growth, development, and evolution. Front Plant Sci 5:445
Mancuso S, Baluŝka F (2017) Plant ocelli for visually guided plant behavior. Trends Plant Sci 22:5–6
Martínez-García JF, Gallemí M, Molina-Contreras MJ, Llorente B, Bevilaqua MRR, 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
Matsuda S, Kajizuka T, Kadota A, Nishimura T, Koshiba T (2011) NPH3-and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles. J Exp Bot 62:3459–3466
Nagatani A (2004) Light-regulated nuclear localization of phytochromes. Curr Opin Plant Biol 7:708–711
Nakasako M, Zikihara K, Matsuoka D, Katsura H, Tokutomi S (2008) Structural basis of the LOV1 dimerization of Arabidopsis phototropins 1 and 2. J Mol Biol 381:718–733
Nakasone Y, Zikihara K, Tokutomi S, Terazima M (2013) Photochemistry of Arabidopsis phototropin 1 LOV1: transient tetramerization. Photochem Photobiol Sci USA 12:1171–1179
Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S, Silva J et al (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119
Nilsson T, Daniel G (2014) Developments in the study of soft rot and bacterial decay. In: Forest products biotechnology. CRC Press, Boca Raton, pp 47–72
Occhipinti A, De Santis A, Maffei ME (2014) Magnetoreception: an unavoidable step for plant evolution? Trends Plant Sci 19:1–4
Oide M, Okajima K, Nakagami H, Kato T, Sekiguchi Y, Oroguchi T et al (2018) Blue light-excited LOV1 and LOV2 domains cooperatively regulate the kinase activity of full-length phototropin2 from Arabidopsis. J Biol Chem 293:963–972
Osugi A, Itoh H, Ikeda-Kawakatsu K, Takano M, Izawa T (2011) Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol 157:1128–1137
Paik I, Yang S, Choi G (2012) Phytochrome regulates translation of mRNA in the cytosol. Proc Natl Acad Sci U S A 109:1335–1340
Park E, Park J, Kim J, Nagatani A, Lagarias JC, Choi G (2012) Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J 72:537–546
Pedmale UV, Liscum E (2007) Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3. J Biol Chem 282:19992–20001
Pedmale UV, Huang SC, Zander M, Cole BJ, Hetzel J, Ljung K et al (2016) Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell 164:233–245
Pfeifer A, Mathes T, Lu Y, Hegemann P, Kottke T (2010) Blue light induces global and localized conformational changes in the kinase domain of full-length phototropin. Biochemistry 49:1024–1032
Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiol 176:1025–1038
Platt TG, Bever JD (2009) Kin competition and the evolution of cooperation. Trends Ecol Evol 24:370–377
Preuten T, Hohm T, Bergmann S, Fankhauser C (2013) Defining the site of light perception and initiation of phototropism in Arabidopsis. Curr Biol 23:1934–1938
Preuten T, Blackwood L, Christie JM, Fankhauser C (2015) Lipid anchoring of Arabidopsis phototropin 1 to assess the functional significance of receptor internalization: should I stay or should I go? New Phytol 206:1038–1050
Rakusová H, Fendrych MÅ, Friml J (2015) Intracellular trafficking and PIN-mediated cell polarity during tropic responses in plants. Curr Opin Plant Biol 23:116–123
Ritz T, Yoshii T, Foerster C, Ahmad M (2010) Cryptochrome: a photoreceptor with the properties of a magnetoreceptor? Commun Integr Biol 3:24–27
Rizzini L, Favory J, Cloix C, Faggionato D, O’Hara A, Kaiserli E et al (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR et al (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci U S A 98:6969–6974
Salomon M, Zacherl M, Rudiger W (1997) Phototropism and protein phosphorylation in higher plants: unilateral blue light irradiation generates a directional gradient of protein phosphorylation across the oat coleoptile. Plant Biol 110:214–216
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265
Sharma R, López-Juez E, Nagatani A, Furuya M (1993) Identification of photo-inactive phytochrome A in etiolated seedlings and photo-active phytochrome B in green leaves of the aurea mutant of tomato. Plant J 4:1035–1042
Sharma S, Kharshiing E, Srinivas A, Zikihara K, Tokutomi S, Nagatani A et al (2014) A dominant mutation in the light-oxygen and voltage2 domain vicinity impairs phototropin1 signaling in tomato. Plant Physiol 164:2030–2044
Shen Y, Khanna R, Carle CM, Quail PH (2007) Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol 145:1043–1051
Sinclair SA, Larue C, Bonk L, Khan A, Castillo-Michel H, Stein RJ et al (2017) Etiolated seedling development requires repression of photomorphogenesis by a small cell-wall-derived dark signal. Curr Biol 27:3403–3418
Song YH, Smith R, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049
Song J, Liu Q, Hu B, Wu W (2017) Photoreceptor PhyB involved in Arabidopsis temperature perception and heat-tolerance formation. Int J Mol Sci 18:1194
Srinivas A, Behera RK, Kagawa T, Wada M, Sharma R (2004) High pigment1 mutation negatively regulates phototropic signal transduction in tomato seedlings. Plant Physiol 134:790–800
Sullivan S, Hart JE, Rasch P, Walker CH, Christie JM (2016a) Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis. Front Plant Sci 7:290
Sullivan S, Takemiya A, Kharshiing E, Cloix C, Shimazaki KI, Christie JM (2016b) Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex. Plant J 88:907–920
Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A et al (2013a) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094
Takemiya A, Yamauchi S, Yano T, Ariyoshi C, Shimazaki KI (2013b) Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening. Plant Cell Physiol 54:24–35
van Gelderen K, Kang C, Pierik R (2018) Light signaling, root development, and plasticity. Plant Physiol 176:1049–1060
Wang H, Wang H (2015) Phytochrome signaling: time to tighten up the loose ends. Mol Plant 8:540–551
Wang H, Ma L, Li J, Zhao H, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294:154–158
Wang Q, Zuo Z, Wang X, Gu L, Yoshizumi T, Yang Z et al (2016) Photoactivation and inactivation of Arabidopsis cryptochrome 2. Science 354:343–347
Wang X, Wang Q, Han Y, Liu Q, Gu L, Yang Z et al (2017) A CRY-BIC negative-feedback circuitry regulating blue light sensitivity of Arabidopsis. Plant J 92:426–436
West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007) The social lives of microbes. Annu Rev Ecol Evol Syst 38:53–77
Wigge PA (2011) FT, a mobile developmental signal in plants. Curr Biol 21:R374–R378
Xu C, Yin X, Lv Y, Wu C, Zhang Y, Song T (2012) A near-null magnetic field affects cryptochrome-related hypocotyl growth and flowering in Arabidopsis. Adv Space Res 49:834–840
Xu P, Lian H, Wang W, Xu F, Yang H (2016) Pivotal roles of the phytochrome-interacting factors in cryptochrome signaling. Mol Plant 9:496–497
Yang H, Tang R, Cashmore AR (2001) The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 13:2573–2587
Yin R, Skvortsova M, Loubéry S, Ulm R (2016) COP1 is required for UV-B induced nuclear accumulation of the UVR8 photoreceptor. Proc Natl Acad Sci U S A 113:E4415–E4422
Yu X, Sayegh R, Maymon M, Warpeha K, Klejnot J, Yang H et al (2009) Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light dependent degradation. Plant Cell 21:118–130
Zeugner A, Byrdin M, Bouly J, Bakrim N, Giovani B, Brettel K et al (2005) Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J Biol Chem 280:19437–19440
Acknowledgements
EK is supported by grant no. SB/EMEQ-152/2014 from the Science and Engineering Research Board, Government of India. RS and YS are supported by the Department of Biotechnology grant no. BT/COE/34/SP15209/2015 and YS is supported by grant no BT/PR6983/PBD/16/1007/2012.
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Kharshiing, E., Sreelakshmi, Y., Sharma, R. (2019). The Light Awakens! Sensing Light and Darkness. In: Sopory, S. (eds) Sensory Biology of Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-8922-1_2
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