Advertisement

The Light Awakens! Sensing Light and Darkness

  • Eros Kharshiing
  • Yellamaraju Sreelakshmi
  • Rameshwar Sharma
Chapter

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.

Keywords

Cryptochrome Light sensing Photomorphogenesis Phototropism Phytochrome Skotomorphogenesis Shade avoidance UVR8 

Notes

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.

References

  1. Ahmad M, Galland P, Ritz T, Wiltschko R, Wiltschko W (2007) Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225:615–624PubMedCrossRefGoogle Scholar
  2. 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 23:439–446PubMedCrossRefGoogle Scholar
  3. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639PubMedCrossRefGoogle Scholar
  4. Baluška F, Mancuso S (2016) Vision in plants via plant-specific ocelli? Trends Plant Sci 21:727–730PubMedCrossRefGoogle Scholar
  5. 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 282:14916–14922PubMedCrossRefGoogle Scholar
  6. 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 16:1433–1445PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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 282:9383–9391PubMedCrossRefGoogle Scholar
  8. Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210PubMedCrossRefGoogle Scholar
  9. 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 111:10179–10184PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chen M, Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21:664–671PubMedPubMedCentralCrossRefGoogle Scholar
  11. 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 26:640–646PubMedCrossRefGoogle Scholar
  12. 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 143:517–529PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 96:8779–8783PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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:e1001076PubMedPubMedCentralCrossRefGoogle Scholar
  15. 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 335:1492–1496PubMedPubMedCentralCrossRefGoogle Scholar
  16. Christie JM, Blackwood L, Petersen J, Sullivan S (2015) Plant flavoprotein photoreceptors. Plant Cell Physiol 56:401–413PubMedCrossRefGoogle Scholar
  17. Crepy MA, Casal JJ (2015) Photoreceptor-mediated kin recognition in plants. New Phytol 205:329–338PubMedCrossRefGoogle Scholar
  18. 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 31:3457–3467PubMedPubMedCentralCrossRefGoogle Scholar
  19. Demkura PV, Ballaré CL (2012) UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol Plant 5:642–652PubMedCrossRefGoogle Scholar
  20. Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133:1617–1629PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dudley SA, File AL (2007) Kin recognition in an annual plant. Biol Lett 3:435–438PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 28:591–601PubMedPubMedCentralCrossRefGoogle Scholar
  23. Franklin KA (2008) Shade avoidance. New Phytol 179:930–944PubMedCrossRefGoogle Scholar
  24. 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 108:20231–20235PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 114:9206–9211PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gianoli E (2017) Eyes in the chameleon vine? Trends Plant Sci 22:4–5PubMedCrossRefGoogle Scholar
  27. Gianoli E, Carrasco-Urra F (2014) Leaf mimicry in a climbing plant protects against herbivory. Curr Biol 24:984–987PubMedCrossRefGoogle Scholar
  28. Giovani B, Byrdin M, Ahmad M, Brettel K (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat Struct Mol Biol 10:489–490CrossRefGoogle Scholar
  29. Goyal A, Karayekov E, Galvão VC, Ren H, Casal JJ, Fankhauser C (2016) Shade promotes phototropism through phytochrome B-controlled auxin production. Curr Biol 26:3280–3287PubMedCrossRefGoogle Scholar
  30. Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot 103:1165–1172PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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 37:1688–1702PubMedCrossRefGoogle Scholar
  32. Haberlandt G (1905) Die Lichtsinnesorgane der Laubblätter. W. Engelmann, LeipzigGoogle Scholar
  33. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 10:751PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 24:4590–4606PubMedPubMedCentralCrossRefGoogle Scholar
  36. 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:e1004218PubMedPubMedCentralCrossRefGoogle Scholar
  37. Inoue S, Kinoshita T (2008) Blue light regulation of stomatal opening and the plasma membrane H+-ATPase. Plant Physiol 174:531–538CrossRefGoogle Scholar
  38. Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582PubMedCrossRefGoogle Scholar
  39. 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 42:635PubMedCrossRefGoogle Scholar
  40. Iwabuchi K, Minamino R, Takagi S (2010) Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis leaf cells. Plant Physiol 152:1309–1319PubMedPubMedCentralCrossRefGoogle Scholar
  41. 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):6405–6414PubMedCrossRefPubMedCentralGoogle Scholar
  42. 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 291:2138–2141PubMedCrossRefGoogle Scholar
  43. 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 285:34765–34772PubMedPubMedCentralCrossRefGoogle Scholar
  44. 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 109:11217–11221PubMedPubMedCentralCrossRefGoogle Scholar
  45. 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:ra106PubMedCrossRefGoogle Scholar
  46. 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 8:2259PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 354:897–900PubMedCrossRefGoogle Scholar
  48. Legris M, Nieto C, Sellaro R, Prat S, Casal JJ (2017) Perception and signalling of light and temperature cues in plants. Plant J 90:683–697PubMedCrossRefGoogle Scholar
  49. Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26:56–78PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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 20:337–352PubMedPubMedCentralCrossRefGoogle Scholar
  51. Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272:398–401PubMedCrossRefGoogle Scholar
  52. Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. The Arabidopsis Book, American Society for Plant Biologists, RockvilleCrossRefGoogle Scholar
  53. 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 25:1023–1028PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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–S162PubMedCrossRefGoogle Scholar
  55. 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 269:968–970PubMedCrossRefGoogle Scholar
  56. 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 110:17582–17587PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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 109:4774–4779PubMedPubMedCentralCrossRefGoogle Scholar
  58. Maffei ME (2014) Magnetic field effects on plant growth, development, and evolution. Front Plant Sci 5:445PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mancuso S, Baluŝka F (2017) Plant ocelli for visually guided plant behavior. Trends Plant Sci 22:5–6PubMedCrossRefGoogle Scholar
  60. 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:e109275PubMedPubMedCentralCrossRefGoogle Scholar
  61. 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 62:3459–3466PubMedPubMedCentralCrossRefGoogle Scholar
  62. Nagatani A (2004) Light-regulated nuclear localization of phytochromes. Curr Opin Plant Biol 7:708–711PubMedCrossRefGoogle Scholar
  63. 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 381:718–733PubMedCrossRefGoogle Scholar
  64. Nakasone Y, Zikihara K, Tokutomi S, Terazima M (2013) Photochemistry of Arabidopsis phototropin 1 LOV1: transient tetramerization. Photochem Photobiol Sci USA 12:1171–1179CrossRefGoogle Scholar
  65. 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 478:119PubMedCrossRefGoogle Scholar
  66. Nilsson T, Daniel G (2014) Developments in the study of soft rot and bacterial decay. In: Forest products biotechnology. CRC Press, Boca Raton, pp 47–72Google Scholar
  67. Occhipinti A, De Santis A, Maffei ME (2014) Magnetoreception: an unavoidable step for plant evolution? Trends Plant Sci 19:1–4PubMedCrossRefGoogle Scholar
  68. 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 293:963–972PubMedCrossRefGoogle Scholar
  69. 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 157:1128–1137PubMedPubMedCentralCrossRefGoogle Scholar
  70. Paik I, Yang S, Choi G (2012) Phytochrome regulates translation of mRNA in the cytosol. Proc Natl Acad Sci U S A 109:1335–1340PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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 72:537–546PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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 282:19992–20001PubMedCrossRefGoogle Scholar
  73. 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 164:233–245PubMedCrossRefGoogle Scholar
  74. 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 49:1024–1032PubMedCrossRefGoogle Scholar
  75. Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiol 176:1025–1038PubMedCrossRefGoogle Scholar
  76. Platt TG, Bever JD (2009) Kin competition and the evolution of cooperation. Trends Ecol Evol 24:370–377PubMedPubMedCentralCrossRefGoogle Scholar
  77. Preuten T, Hohm T, Bergmann S, Fankhauser C (2013) Defining the site of light perception and initiation of phototropism in Arabidopsis. Curr Biol 23:1934–1938PubMedCrossRefGoogle Scholar
  78. 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 206:1038–1050PubMedCrossRefGoogle Scholar
  79. Rakusová H, Fendrych MÅ, Friml J (2015) Intracellular trafficking and PIN-mediated cell polarity during tropic responses in plants. Curr Opin Plant Biol 23:116–123PubMedCrossRefGoogle Scholar
  80. Ritz T, Yoshii T, Foerster C, Ahmad M (2010) Cryptochrome: a photoreceptor with the properties of a magnetoreceptor? Commun Integr Biol 3:24–27PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 332:103–106PubMedCrossRefGoogle Scholar
  82. 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 98:6969–6974PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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 110:214–216Google Scholar
  84. Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 4:1035–1042PubMedCrossRefGoogle Scholar
  86. 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 164:2030–2044PubMedPubMedCentralCrossRefGoogle Scholar
  87. Shen Y, Khanna R, Carle CM, Quail PH (2007) Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol 145:1043–1051PubMedPubMedCentralCrossRefGoogle Scholar
  88. 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 27:3403–3418PubMedCrossRefGoogle Scholar
  89. Song YH, Smith R, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049PubMedPubMedCentralCrossRefGoogle Scholar
  90. Song J, Liu Q, Hu B, Wu W (2017) Photoreceptor PhyB involved in Arabidopsis temperature perception and heat-tolerance formation. Int J Mol Sci 18:1194PubMedCentralCrossRefPubMedGoogle Scholar
  91. Srinivas A, Behera RK, Kagawa T, Wada M, Sharma R (2004) High pigment1 mutation negatively regulates phototropic signal transduction in tomato seedlings. Plant Physiol 134:790–800PubMedPubMedCentralCrossRefGoogle Scholar
  92. 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 7:290PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 88:907–920PubMedPubMedCentralCrossRefGoogle Scholar
  94. 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 4:2094PubMedCrossRefGoogle Scholar
  95. 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 54:24–35PubMedCrossRefGoogle Scholar
  96. van Gelderen K, Kang C, Pierik R (2018) Light signaling, root development, and plasticity. Plant Physiol 176:1049–1060PubMedCrossRefGoogle Scholar
  97. Wang H, Wang H (2015) Phytochrome signaling: time to tighten up the loose ends. Mol Plant 8:540–551PubMedCrossRefGoogle Scholar
  98. Wang H, Ma L, Li J, Zhao H, Deng XW (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294:154–158PubMedCrossRefGoogle Scholar
  99. Wang Q, Zuo Z, Wang X, Gu L, Yoshizumi T, Yang Z et al (2016) Photoactivation and inactivation of Arabidopsis cryptochrome 2. Science 354:343–347PubMedPubMedCentralCrossRefGoogle Scholar
  100. 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 92:426–436PubMedPubMedCentralCrossRefGoogle Scholar
  101. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007) The social lives of microbes. Annu Rev Ecol Evol Syst 38:53–77CrossRefGoogle Scholar
  102. Wigge PA (2011) FT, a mobile developmental signal in plants. Curr Biol 21:R374–R378PubMedCrossRefGoogle Scholar
  103. 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 49:834–840CrossRefGoogle Scholar
  104. Xu P, Lian H, Wang W, Xu F, Yang H (2016) Pivotal roles of the phytochrome-interacting factors in cryptochrome signaling. Mol Plant 9:496–497PubMedCrossRefGoogle Scholar
  105. Yang H, Tang R, Cashmore AR (2001) The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 13:2573–2587PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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–E4422PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 21:118–130PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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 280:19437–19440PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Eros Kharshiing
    • 1
  • Yellamaraju Sreelakshmi
    • 2
  • Rameshwar Sharma
    • 2
  1. 1.Department of BotanySt. Edmund’s CollegeMeghalayaIndia
  2. 2.Repository of Tomato Genomics ResourcesUniversity of HyderabadHyderabadIndia

Personalised recommendations