Молекулярные основы сигнальных процессов, регулируемых сенсорными фоторецепторами криптохромами у растений

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Аннотация

Сенсоры синего света, криптохромы, составляют широко распространённый класс флавопротеиновых фоторецепторов, которые у растений регулируют сигнальные процессы, лежащие в основе их развития, роста и метаболизма. У некоторых водорослей криптохромы могут действовать не только как сенсорные фоторецепторы, но также как фотолиазы, катализирующие репарацию УФ-индуцированных повреждений ДНК. Криптохромы связывают в качестве хромофора FAD в гомологичном фотолиазе домене (photolyase homologous region, PHR) и содержат C-концевое удлинение (cryptochrome C-terminal extension, CCE), отсутствующее у фотолиаз. Фотосенсорный процесс в криптохроме инициируется фотохимическими превращениями хромофора, включающими образование редокс-форм FAD. В состоянии с восстановленным до нейтрального радикала хромофором (FADH•) фоторецепторный белок подвергается фосфорилированию, конформационному изменению и разобщению PHR-домена и CCE с последующим формированием олигомеров криптохромных молекул. Фотоолигомеризация - структурная основа функциональной активности криптохромов, определяющая формирование их комплексов с разнообразными сигнальными белками, включая транскрипционные факторы и регуляторы транскрипции. Взаимодействия в таких комплексах изменяют активность сигнальных белков, что приводит к регуляции экспрессии генов и фотоморфогенезу растений. В последнее время опубликовано много работ с новой, более детальной информацией о молекулярных механизмах отмеченных выше процессов. В настоящем обзоре основное внимание сосредоточено на анализе данных этих публикаций, особенно касающихся структурных аспектов перехода криптохромов в фотоактивированное состояние и регуляторных сигнальных процессов, опосредуемых криптохромными фоторецепторами у растений.

Об авторах

Г. Я Фрайкин

Московский государственный университет имени М.В. Ломоносова

Email: Gfraikin@yandex.ru
119991 Москва, Россия

Н. С Беленикина

Московский государственный университет имени М.В. Ломоносова

119991 Москва, Россия

А. Б Рубин

Московский государственный университет имени М.В. Ломоносова

119991 Москва, Россия

Список литературы

  1. Losi, A., and Gartner, W. (2012) The evolution of flavin-binding photoreceptors: an ancient chromophore serving trendy blue-light sensors, Annu. Rev. Plant Biol., 63, 49-72, doi: 10.1146/annurev-arplant-042811-105538.
  2. Fraikin, G. Ya., Strakhovskaya, M. G., and Rubin, A. B. (2013) Biological photoreceptors of light-dependent regulatory processes, Biochemistry (Moscow), 78, 1238-1253, doi: 10.1134/S0006297913110047.
  3. Li, F.-W., and Mathews, S. (2016) Evolutionary aspects of plant photoreceptors, J. Plant Res., 129, 115-122, doi: 10.1007/s10265-016-0785-4.
  4. Podolec, R., Demarsy, E., and Ulm, R. (2021) Perception and signaling of ultraviolet-B radiation in plants, Annu. Rev. Plant Biol., 72, 793-822, doi: 10.1146/annurev-arplant-050718-095946.
  5. Inoue, K., Nishihama, R., and Kohchi, T. (2017) Evolutionary origin of phytochrome responses and signaling in land plants, Plant Cell Environ., 40, 2502-2508, doi: 10.1111/pce.12908.
  6. Fraikin, G. Ya., Strakhovskaya, M. G., Belenikina, N. S., and Rubin, A. B. (2015) Bacterial photosensory proteins: regulatory functions and optogenetic applications, Microbiology, 84, 461-472, doi: 10.1134/S0026261715040086.
  7. Demarsy, E., Goldschmidt-Clemont, M., and Ulm, R. (2018) Coping with "dark sides of the sun" through photoreceptor signaling, Trends Plant Sci., 23, 260-271, doi: 10.1016/j.tplants.2017.11.007.
  8. Фрайкин Г. Я. (2018) Белковые сенсоры света: фотовозбуждённые состояния, сигнальные свойства и применение в оптогенетике, АР-Консалт, Москва.
  9. Ponnu, J., and Hoecker, U. (2022) Signaling mechanisms by Arabidopsis cryptochromes, Front. Plant Sci., 13, 844714, doi: 10.3389/fpls.2022.844714.
  10. Vechtomova, Y. L., Telegina, T. A., and Kritsky, M. S. (2020) Evolution of proteins of the DNA photolyase/cryptochrome family, Biochemistry (Moscow), 85 (Suppl. 1), S131-S153, doi: 10.1134/S0006297920140072.
  11. Wang, Q., and Lin, C. (2020) Mechanisms of cryptochrome-mediated photoresponses in plants, Annu. Rev. Plant Biol., 71, 103-129, doi: 10.1146/annurev-arplant-050718-100300.
  12. Fraikin, G. (2017) Photobioregulatory Receptors, Lambert Academic Publishing, Saarbrucken.
  13. Sun, K., and Zhu, Z. (2018) Illuminating the nucleus: UVR8 interacts with more, Trends Plant Sci., 23, 279-281, doi: 10.1016/j.tplants.2018.03.002.
  14. Ahmad, M. (2016) Photocycle and signaling mechanisms of plant cryptochromes, Curr. Opin. Plant Biol., 33, 108-115, doi: 10.1016/j.pbi.2016.06.013.
  15. Christie, J. M., Blackwood, L., Petersen, J., and Sullivan, S. (2015) Plant flavoprotein photoreceptors, Plant Cell Physiol., 56, 401-413, doi: 10.1093/pcp/pcu196.
  16. Фрайкин Г. Я., Рубин А. Б. (2022) В кн. Горизонты биофизики. Т. 1 (под ред. Рубина А. Б.), Институт компьютерных исследований, М.-Ижевск, с. 426-454.
  17. Cheng, M. C., Kathare, P. K., Paik, I., and Huq, E. (2021) Phytochrome signaling networks, Annu. Rev. Plant Biol., 72, 217-244, doi: 10.1146/annurev-arplant-080620-024221.
  18. Bae, G., and Choi, G. (2008) Decoding of light signals by plant phytochromes and their interacting proteins, Annu. Rev. Plant Biol., 59, 281-311, doi: 10.1146/annurev.arplant.59.032607.092859.
  19. Franklin, K. A., and Quail, P. H. (2010) Phytochrome functions in Arabidopsis development, J. Exp. Bot., 61, 11-24, doi: 10.1093/jxb/erp304.
  20. Fraser, D. P., Hayes, S., and Franklin, K. A. (2016) Photoreceptor crosstalk in shade avoidance, Curr. Opin. Plant Biol., 33, 1-7, doi: 10.1016/jpbi.2016.03.008.
  21. Chen, M., and Chory, J. (2011) Phytochrome signaling mechanisms and the control of plant development, Trends Cell Biol., 21, 664-671, doi: 10.1016/j.tcb.2011.07.002.
  22. Pham, V. N., Kathare, P. K., and Huq, E. (2018) Phytochromes and phytochrome interacting factors, Plant Physiol., 176, 1025-1038, doi: 10.1104/pp.17.01384.
  23. Wang, Q., Zuo, Z., Wang, X., Liu, Q., Gu, L., Oka, Y., and Lin, C. (2018) Beyond the photocycle - how cryptochromes regulate photoresponses in plants? Curr. Opin. Plant Biol., 45, 120-126, doi: 10.1016/j.pbi.2018.05.014.
  24. Demarsy, E., and Fankhauser, C. (2009) Higher plants use LOV to perceive blue light, Curr. Opin. Plant Biol., 12, 69-74, doi: 10.1016/j.pbi.2008.09.002.
  25. Christie, J. M., Arvai, A. S., Baxter, K. J., Heilmann, M., Pratt, A. J., O'Hara, A., Kelly, S. M., Hothorn, M., Smith, B. O., Hitomi, K., Jenkins, G. I., and Getzoff, E. D. (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges, Science, 335, 1492-1496, doi: 10.1126/science.1218091.
  26. Fraikin, G. Ya. (2018) Signaling mechanisms regulating diverse plant cell responses to UVB radiation, Biochemistry (Moscow), 83, 787-794, doi: 10.1134/S0006297918070027.
  27. Rockwell, N. C., Shang, L., Martin, S. S., and Lagarias, J. C. (2009) Distinct classes of red/far-red photochemistry within the phytochrome superfamily, Proc. Natl. Acad. Sci. USA, 106, 6123-6127, doi: 10.1073/pnas.0902370106.
  28. Schwinn, K., Ferre, N., and Huix-Rotllant, M. (2020) UV-visible absorption spectrum of FAD and its reduced forms embedded in a cryptochrome protein, Phys. Chem. Chem. Phys., 22, 12447-12455, doi: 10.1039/d0cp01714k.
  29. Fraikin, G. Ya. (2022) Photosensory and signaling properties of cryptochromes, Mosc. Univ. Biol. Sci. Bull., 77, 54-63, doi: 10.3103/S0096392522020031.
  30. Ahmad, M., and Cashmore, A. R. (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor, Nature, 366, 162-166, doi: 10.1038/366162a0.
  31. Sancar, A. (2004) Photolyase and cryptochrome blue-light photoreceptors, Adv. Protein Chem., 69, 73-100, doi: 10.1016/S0065-3233(04)69003-6.
  32. Cashmore, A. R., Jarillo, J. A., Wu, Y. J., and Liu, D. (1999) Cryptochromes: blue light receptors for plants and animals, Science, 284, 760-765, doi: 10.1126/science.284.5415.760.
  33. Muller, M., and Carell, T. (2009) Structural biology of DNA photolyases and cryptochromes, Curr. Opin. Struct. Biol., 19, 277-285, doi: 10.1016/j.sbi.2009.05.003.
  34. Zoltowski, B. D. (2015) Resolving cryptic aspects of cryptochrome signaling, Proc. Natl. Acad. Sci. USA, 112, 8811-8812, doi: 10.1073/pnas.1511092112.
  35. Takahashi, J. S. (2017) Transcriptional architecture of the mammalian circadian clock, Nat. Rev. Genet., 18, 164-179, doi: 10.1038/nrg.2016.150.
  36. Wu, G., and Spalding, E. P. (2007) Separate functions for nuclear and cytoplasmic cryptochrome 1 during photomorphogenesis of Arabidopsis seedlings, Proc. Natl. Acad. Sci. USA, 104, 18813-18818, doi: 10.1073/pnas.0705082104.
  37. Yu, X., Klejnot, J., Zhao, X., Shalitin, D., Maymon, M., Yang, H., Lee, J., Liu, X., Lopez, J., and Lin, C. (2007) Arabidopsis cryptochrome 2 completes its posttranslational life cycle in the nucleus, Plant Cell, 19, 3146-3156, doi: 10.1105/tpc.107.053017.
  38. Pooam, M., Arthaut, L.-D., Burdick, D., Link, J., Martino, C. F., and Ahmad, M. (2019) Magnetic sensitivity mediated by the Arabidopsis blue-light receptor cryptochrome occurs during flavin reoxidation in the dark, Planta, 249, 319-332, doi: 10.1007/s00425-018-3002-y.
  39. Zoltowski, B. D., Chelliah, Y., Wickramaratne, A., Jarecha, L., Karki, N., Xu, W., Mouritsen, H., Hore, P. J., Hibbs, R. E., Green, C. B., and Takahashi, J. S. (2019) Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon, Proc. Natl. Acad. Sci. USA, 116, 19449-19457, doi: 10.1073/pnas.1907875116.
  40. Petersen, J., Rredhi, A., Szyttenholm, J., Oldemeyer, S., Kottke, T., and Mittag, M. (2021) The world of algae reveals a broad variety of cryptochrome properties and functions, Front. Plant Sci., 12, 748760, doi: 10.3389/fpls.2021.766509.
  41. Palayam, M., Ganapathy, J., Guercio, A. M., Tal, L., Deck, S. L., and Shabek, K. N. (2021) Structural insights into photoactivation of plant cryptochrome-2, Commun. Biol., 4, 28, doi: 10.1038/s42003-020-01531-x.
  42. Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L.-O., van der Horst, G. T., Batschauer, A., and Ahmad, M. (2011) The cryptochromes: blue light photoreceptors in plants and animals, Annu. Rev. Plant Biol., 62, 335-364, doi: 10.1146/annurev-arplant-042110-103759.
  43. Ozturk, N. (2017) Phylogenetic and functional classification of the photolyase/cryptochrome family, Photochem. Photobiol., 93, 1-22, doi: 10.1111/php.12676.
  44. Zhang, M., Wang, L., and Zhong, D. (2017) Photolyase: dynamics and electron-transfer mechanisms of DNA repair, Arch. Biochem. Biophys., 632, 158-174, doi: 10.1016/j.abb.2017.08.007.
  45. Bayram, O., Braus, G. H., Fischer, R., and Rodriguez-Romero, J. (2010) Spotlight on Aspergillus nidulands photosensory systems, Fungal Genet. Biol., 47, 900-908, doi: 10.1016/j.fgb.2010.05.008.
  46. Konig, S., Juhas, M., Jager, S., Kottke, T., and Buchel, C. (2017) The cryptochrome-photolyase protein family in diatoms, J. Plant Physiol., 217, 15-19, doi: 10.1016/j.plph.2017.06.015.
  47. Kottke, T., Oldemeyer, S., Wenzel, S., Zou, Y., and Mittag, M. (2017) Cryptochrome photoreceptors in green algae: unexpected versatility of mechanisms and functions, J. Plant Physiol., 217, 4-14, doi: 10.1016/j.plph.2017.05.021.
  48. Michael, A. K., Fribourgh, J. L., Van Gelder, R. N., and Partch, C. L. (2017) Animal cryptochromes: divergent roles in light perception, circadian timekeeping and beyond, Photochem. Photobiol., 93, 128-140, doi: 10.1111/php.12677.
  49. Oldemeyer, S., Franz, S., Wenzel, S., Essen, L.-O., Mittag, M., and Kottke, T. (2016) Essential role of an unusual long-lived tyrosil radical in the response to red light of the animal-like cryptochrome aCRY, J. Biol. Chem., 291, 14062-14071, doi: 10.1074/jbc.M116.726976.
  50. Paulus, B., Bajzath, C., Melin, F., Heidinger, L., Kromm, V., Herkersdorf, C., Benz, U., Mann, L., Stehle, P., Hellwig, P., Weber, S., and Schleicher, E. (2015) Spectroscopic characterization of radicals and radical pairs in fruit fly cryptochrome - protonated and nonprotonated flavin radical-states, FEBS J., 282, 3175-3189, doi: 10.1111/febs.13299.
  51. Zoltowski, B. D., Vaidya, A. T., Top, D., Widom, J., Young, M. W., and Crane, B. R. (2011) Structure of full-length Drosophila cryptochrome, Nature, 480, 396-399, doi: 10.1038/nature10618.
  52. Sancar, A. (2008) Structure and function of photolyase and in vivo enzymology: 50th anniversary, J. Biol. Chem., 283, 32153-32157, doi: 10.1074/jbc.R800052200.
  53. Franz, S., Ignatz, E., Wenzel, S., Zielosko, H., Putu, E., Maestre-Reyna, M., Tsai, M.-D., Yamomoto, J., Mittag, M., and Essen, L.-O. (2018) Structure of the bifunctional cryptochrome aCRY from Chlamydomonas reinhardtii, Nucleic Acids Res., 46, 8010-8022, doi: 10.1093/nar/gky621.
  54. Hense, A., Herman, E., Oldemeyer, S., and Kottke, T. (2015) Proton transfer to flavin stabilizes the signaling state of the blue light receptor plant cryptochrome, J. Biol. Chem., 290, 1743-1751, doi: 10.1074/jbc.M114.606327.
  55. Lacombat, F., Espagne, A., Dozova, N., Plaza, P., Muller, P., Brettel, K., Franz-Badur, S., and Essen, L.-O. (2019) Ultrafast oxidation of a tyrosine by proton-coupled electron transfer promotes light activation of an animal-like cryptochrome, J. Am. Chem. Soc., 141, 13394-13409, doi: 10.1021/jacs.9b03680.
  56. Oldemeyer, S., Haddat, A. Z., and Fleming, G. R. (2020) Interconnection of the antenna pigment 8-HDF and flavin facilitates red-light reception in bifunctional animal-like cryptochrome, Biochemistry, 59, 594-604, doi: 10.1021/acs.biochem.9b00875.
  57. Goett-Zink, L., and Kottke, T. (2021) Plant cryptochromes illuminated: a spectroscopic perspective on the mechanism, Front. Chem., 9, 780199, doi: 10.3389/fchem.2021.780199.
  58. Thoing, C., Oldemeyer, S., and Kottke, T. (2015) Microsecond deprotonation of aspartic acid and response of the α/β subdomain precede C-terminal signaling in the blue light sensor plant cryptochrome, J. Am. Chem. Soc., 137, 5990-5999, doi: 10.1021/jacs.5b01404.
  59. Herbel, V., Orth, C., Wenzel, R., Ahmad, M., Bittl, R., and Batschauer, A. (2013) Lifetimes of Arabidopsis cryptochrome signaling states in vivo, Plant J., 74, 583-592, doi: 10.1111/tpj.12144.
  60. Muller, P., and Ahmad, M. (2011) Light-activated cryptochrome reacts with molecular oxygen to form a flavin-superoxide radical pair consistent with magnetoreception, J. Biol. Chem., 286, 21033-21040, doi: 10.1074/jbc.M111.228940.
  61. Goett-Zink, L., Toschke, A. L., Petersen, J., Mittag, M., and Kottke, T. (2021) C-terminal extension of plant cryptochrome dissociates from the β-sheet of the flavin-binding domain, J. Phys. Chem. Lett., 12, 5558-5563, doi: 10.1021/acs.jpclett.1c00844.
  62. Liu, Q., Su, T., He, W., Ren, H., Liu, S., Chen, Y., Gao, L., Hu, X., Lu, H., Cao, S., Huang, Y., Wang, X., Wang, Q., and Lin, C. (2020) Photooligomerization determines photosensitivity and photoreactivity of plant cryptochromes, Mol. Plant., 13, 398-413, doi: 10.1016/j.molp.2020.01.002.
  63. Yang, Z., Liu, B., Su, J., Liao, J., Lin, C., and Oka, Y. (2017) Cryptochromes orchestrate transcription regulation of diverse blue light responses in plants, Photochem. Photobiol., 93, 112-127, doi: 10.1111/php.12663.
  64. Wang, Q., and Lin, C. (2020) A structural view of plant CRY2 photoactivation and inactivation, Nat. Struct. Mol. Biol., 27, 401-403, doi: 10.1038/s41594-020-0432-6.
  65. Gao, J., Wang, X., Zhang, M., Bian, M., Deng, W., Zuo, Z., Yang, Z., Zhong, D., and Lin, C. (2015) Trp triad-dependent rapid photoreduction is not required for the function of Arabidopsis CRY1, Proc. Natl. Acad. Sci. USA, 112, 9135-9140, doi: 10.1073/pnas.1504404112.
  66. Liu, H., Su, T., He, W., Wang, G., and Lin, C. (2020) The universally conserved residues are not universally required for stable protein expression or functions of cryptochromes, Mol. Biol. Evol., 37, 327-340, doi: 10.1093/molbev/msz217.
  67. Shao, K., Zhang, X., Li, X., Hao, Y., Huang, X., Ma, M., Zhang, M., Yu, F., Liu, H., and Zhang, P. (2020) The oligomeric structures of plant cryptochromes, Nat. Struct. Mol. Biol., 27, 480-488, doi: 10.1038/s41594-020-0420-x.
  68. Wang, Q., Zuo, Z., Wang, X., Gu, L., Koshizumi, T., Yang, Z., Yang, L., Liu, Q., Liu, W., Han, Y. J., Kim, J. I., Liu, B., Wohlschlegel, J. A., Matsui, M., Oka, Y., and Lin, C. (2016) Photoactivation and inactivation of Arabidopsis cryptochrome 2, Science, 354, 343-347, doi: 10.1126/science.aaf9030.
  69. Ma, L., Wang, X., Guan, Z., Wang, L., Wang, Y., Zheng, L., Gong, Z., Shen, C., Wang, J., Zhang, D., Liu, Z., and Yin, P. (2020) Structural insight into BIC-mediated inactivation of Arabidopsis cryptochrome 2, Nat. Struct. Mol. Biol., 27, 472-479, doi: 10.1038/s41594-020-0410-z.
  70. Liu, H., Yu, X., Li, K., Klejnot, J., Yang, H., Lisiero, D., and Lin, C. (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis, Science, 322, 1535-1539, doi: 10.1126/science.1163927.
  71. Liu, Y., Li, X., Li, K., Lin, H., and Lin, C. (2013) Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis, PLoS Genet., 9, e1003861, doi: 10.1371/journal.pgen.1003861.
  72. Liu, Y., Li, X., Ma, D., Chen, Z., Wang, J.-W., and Liu, H. (2018) CIB and CO interact to mediate CRY2-dependent regulation of flowering, EMBO Rep., 19, e45762, doi: 10.15252/embr.2018.45762.
  73. Ma, D., Li, X., Guo, Y., Chu, J., Fang, S., Yan, C., Noel, J. P., and Liu, H. (2016) Cryptochrome 1 interacts with PIFs to regulate high temperature-mediated hypocotyl elongation in response to blue light, Proc. Natl. Acad. Sci. USA, 113, 224-229, doi: 10.1073/pnas.1511437113.
  74. Pedmale, U. V., Huang, S. C., Zander, M., Cole, B. J., Herzel, J., Nery, J. R., and Ecker, J. R. (2016) Cryptochromes interact directly with PIFs to control plant growth in limiting blue light, Cell, 164, 233-245, doi: 10.1016/j.cell.2015.12.018.
  75. Ni, W., Xu, S.-L., Gonzalez-Grandio, E., Chalkley, R. J., Huhmer, A. F. R., Burlingame, A. L., Wang, Z.-Y., and Qual, P. H. (2017) PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3, Nat. Commun., 8, 15236, doi: 10.1038/ncomms15236.
  76. Castillon, A., Shen, H., and Huq, E. (2009) Blue light induces degradation of the negative regulator phytochrome interacting factor 1 to promote photomorphogenic development of Arabidopsis seedlings, Genetics, 182, 161-171, doi: 10.1534/genetics.108.099887.
  77. Shalitin, D., Yang, H., Mockler, T. C., Maymon, M., Guo, H., Whitelam, G. C., and Lin, C. (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation, Nature, 417, 763-767, doi: 10.1038/nature00815.
  78. Shalitin, D., Yu, X., Maymon, M., Mockler, T., and Lin, C. (2003) Blue-light-dependent in vivo and in vitro phosphorylation of Arabidopsis cryptochrome 1, Plant Cell, 15, 2421-2429, doi: 10.1105/tpc.013011.
  79. Weidler, G., zur Oven-Krockhaus, S., Heunemann, M., Orth, C., Schleifenbaum, F., Harter, K., Hoecker, U., and Batschauer, A. (2012) Degradation of Arabidopsis CRY2 is regulated by SPA proteins and phytochrome A, Plant Cell, 24, 2610-2623, doi: 10.1105/tpc.112.098210.
  80. Liu, Q., Wang, Q., Liu, B., Wang, W., Wang, X., Park, J., Yang, Z., Du, X., Bian, M., and Lin, C. (2016) The blue-light-dependent polyubiquitination and degradation of Arabidopsis cryptochrome 2 requires multiple E3 ubiquitin ligases, Plant Cell Physiol., 57, 2175-2186, doi: 10.1093/pcp/pcw134.
  81. Liu, Q., Wang, Q., Deng, W., Wang, X., Piao, M., Cai, D., Li, Y., Barshop, W. D., Yu, X., Zhou, T., Liu, B., Oka, Y., Wohlschlegel, J., Zuo, Z., and Lin, C. (2017) Molecular basis for blue light-dependent phosphorylation of Arabidopsis cryptochrome 2, Nat. Commun., 8, 15234, doi: 10.1038/ncomms15234.
  82. Wang, H., Ma, L. G., Li, G. M., Zhao, H. Y., and Deng, X. W. (2001) Direct interaction of Arabidopsis cryptochromes with COP1 in light control development, Science, 294, 154-158, doi: 10.1126/science.1063630.
  83. Yang, H.-Q., Tang, R.-H., and Cashmore, A. R. (2001) The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1, Plant Cell, 13, 2573-2587, doi: 10.1105/tpc.010367.
  84. Ponnu, J. (2020) Molecular mechanisms suppressing COP1/SPA E3 ubiquitin ligase activity in blue light, Physiol. Plant, 169, 418-429, doi: 10.1111/ppl.13103.
  85. Heijde, M., and Ulm, R. (2012) UV-B photoreceptor-mediated signaling in plants, Trends Plant Sci., 17, 230-237, doi: 10.1016/j.tplants.2012.01.007.
  86. Hoecker, U. (2017) The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling, Curr. Opin. Plant Biol., 37, 63-69, doi: 10.1016/j.pbi.2017.03.015.
  87. Podolec, R., and Ulm, R. (2018) Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase, Curr. Opin. Plant Biol., 45, 18-25, doi: 10.1016/j.pbi.2018.04.018.
  88. Paik, I., Chen, F., Ngoc Pham, V., Zhu, L., Kim, J. I., and Huq, E. (2019) A phyB-PIF1-SPA1 kinase regulatory complex promotes photomorphogenesis in Arabidopsis, Nat. Commun., 10, 4216, doi: 10.1038/s41467-019-12110-y.
  89. Wang, W., Paik, I., Kim, J., Hou, X., Sung, S., and Huq, E. (2021) Direct phosphorylation of HY5 by SPA kinases to regulate photomorphogenesis in Arabidopsis, New Phytol., 230, 2311-2326, doi: 10.1111/nph.17332.
  90. Ponnu, J., and Hoecker, U. (2021) Illuminating the COP1/SPA ubiquitin ligase: fresh insight into its structure and functions during plant photomorphogenesis, Front. Plant Sci., 12, 662793, doi: 10.3389/fpls.2021.662793.
  91. Balzerowicz, M., Kemer, K., Schenkel, C., and Hoecker, U. (2017) SPA proteins affect the sub-cellular localization of COP1 in the COP1/SPA ubiquitin ligase complex during photomorphogenesis, Plant Physiol., 174, 1314-1321, doi: 10.1104/pp.17.00488.
  92. Kerner, K., Nagano, S., Lubbe, A., and Hoecker, U. (2021) Functional comparison of the WD-repeat domains of SPA1 and COP1 in suppression of photomorphogenesis, Plant Cell Environ., 44, 3273-3282, doi: 10.1111/pce.14128.
  93. Pacin, M., Legris, M., and Casal, J. J. (2014) Rapid decline in nuclear constitutive photomorphogenesis 1 abundance anticipates the stabilization of its target ELONGATED hypocotyl 5 in the light, Plant Physiol., 164, 1134-1138, doi: 10.1104/pp.113.234245.
  94. Lian, H. L., He, S. B., Zhang, Y. C., Zhu, D. M., Zhang, J. Y., Jia, K. P., San, S. X., Li, L., and Yang, H. Q. (2011) Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism, Genes Dev., 25, 1023-1028, doi: 10.1101/gad.2025111.
  95. Liu, B., Zuo, Z., Liu, H., Liu, X., and Lin, C. (2011) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light, Genes Dev., 25, 1029-1034, doi: 10.1101/gad.2025011.
  96. Zuo, Z., Liu, H., Liu, B., Liu, X., and Lin, C. (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis, Curr. Biol., 21, 841-847, doi: 10.1016/j.cub.2011.03.048.
  97. Holtkotte, X., Ponnu, J., Ahmad, M., and Hoecker, U. (2017) The blue light-induced interaction of cryptochrome 1 with COP1 requires SPA proteins during Arabidopsis light signaling, PLoS Genet., 13, e1007044, doi: 10.1371/journal.pgen.1007044.
  98. Lau, K., Podolec, R., Chappuis, R., Ulm, R., and Hothorn, M. (2019) Plant photoreceptors and their signaling components compete for COP1 binding via VP peptide motifs, EMBO J., 38, e102140, doi: 10.15252/embj.2019102140.
  99. Ponnu, J., Riedel, T., Penner, E., Schrader, A., and Hoecker, U. (2019) Cryptochrome 2 competes with COP1-substrates to repress COP1 ligase activity during Arabidopsis photomorphogenesis, Proc. Natl. Acad. Sci. USA, 116, 27133-27141, doi: 10.1073/pnas.1909181116.

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