Abstract
Reversible protein phosphorylation is a switching mechanism used in eukaryotes to regulate various cellular signalings. In plant light signaling, sophisticated photosensory receptor systems operate to modulate growth and development. The photoreceptors include phytochromes, cryptochromes and phototropins. Despite considerable progresses in defining the photosensory roles of these photoreceptors, the primary biochemical mechanisms by which the photoreceptor molecules transduce the perceived light signals into cellular responses remain to be elucidated. The signal-transducing photoreceptors in plants are all phosphoproteins and/or protein kinases, suggesting that light-dependent protein phosphorylation and dephosphorylation play important roles in the function of the photoreceptors. This review focuses on the role of phytochromes’ reversible phosphorylation involved in the light signal transduction in plants.
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J. C. Watson, Light and protein kinases, Adv. Bot. Res., 2000, 32, 149–184.
S. Luan, Protein phosphatases in plants, Annu. Rev. Plant Biol., 2003, 54, 63–92.
D. Kerk, J. Bulgrien, D. W. Smith, B. Barsam, S. Veretnik and M. Gribskov, The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis, Plant Physiol., 2002, 129, 908–925.
J. H. Tchieu, F. Fana, J. L. Fink, J. Harper, T. M. Nair, R. H. Niedner, D. W. Smith, K. Steube, T. M. Tam, S. Veretnik, D. Wang and M. Gribskov, The PlantsP and PlantsT Functional Genomics Databases, Nucleic Acids Res., 2003, 31, 342–344.
L. N. Johnson, M. O’Reilly, Control by phosphorylation, Curr. Opin. Struct. Biol., 1996, 6, 762–769.
S. Kawakami, H. S. Padgett, D. Hosokawa, Y. Okada, R. N. Beachy and Y. Watanabe, Phosphorylation and/or presence of serine 37 in the movement protein of tomato mosaic tobamovirus is essential for intracellular localization and stability in vivo, J. Virol., 1999, 73, 6831–6840.
T. Pawson, Protein modules and signaling networks, Nature, 1995, 373, 573–580.
G.-Q. Tang, S. C. Hardin, R. Dewey and S. C. Huber, A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds, Plant J., 2003, 34, 77–93.
S. C. Huber and S. C. Hardin, Numerous post-translational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels, Curr. Opin. Plant Biol., 2004, 7, 318–322.
C. S. Hardtke, K. Gohda, M. T. Osterlund, T. Oyama, K. Okada K, X.-W. Deng, HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain, EMBO J., 2000, 19, 4997–5006.
M. M. Neff, C. Fankhauser and J. Chory, Light: an indicator of time and place, Genes Dev., 2000, 14, 257–271.
M. Chen, J. Chory and C. Fankhauser, Light signal transduction in higher plants, Annu. Rev. Genet., 2004, 38, 87–117.
J. A. Sullivan, X.-W. Deng, From seed to seed: the role of photoreceptors in Arabidopsis development, Dev. Biol., 2003, 260, 289–297.
P. H. Quail, M. T. Boylan, B. M. Parks, T. W. Short, Y. Xu and D. Wagner, Phytochromes: Photosensory perception and signal transduction, Science, 1995, 268, 675–680.
J. Chory, M. Chatterjee, R. K. Cook, T. Elich, C. Fankhauser, J. Li, P. Nagpal, M. Neff, A. Pepper, D. Poole, J. Reed and V. Vitart, From seed germination to flowering, light controls plant development via pigment phytochrome, Proc. Natl. Acad. Sci. USA, 1996, 93, 12066–12071.
H. Smith, Phytochromes and light signal perception by plants-an emerging synthesis, Nature, 2000, 407, 585–591.
P. H. Quail, Phytochrome photosensory signaling networks, Nat. Rev. Mol. Cell. Biol., 2002, 3, 85–93.
C. Fankhauser, The phytochromes, a family of red/far-red absorbing photoreceptors, J. Biol. Chem., 2001, 276, 11453–11456.
A. R. Cashmore, J. A. Jarillo JA, Y. J. Wu and D. Liu, Cryptochromes: blue light receptors for plants and animals, Science, 1999, 284, 760–765.
C. Lin and D. Shalitin, Cryptochrome structure and signal transduction, Annu. Rev. Plant Biol., 2003, 54, 469–496.
E. Huala, P. W. Oeller, E. Liscum, I.-S. Han, E. Larsen and W. R. Briggs, Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain, Science, 1997, 278, 2120–2123.
W. R. Briggs and J. M. Christie, Phototropins 1 and 2: versatile plant blue-light receptors, Trends Plant Sci., 2002, 7, 204–210.
N. Datta, Y. R. Chen and S. J. Roux, Phytochrome and calcium stimulation of protein phosphorylation in isolated pea nuclei, Biochim. Biophys. Res. Commun., 1985, 162, 1403–1408.
K. Harter, H. Frohnmeyer, S. Kircher, T. Kunkel, S Muhlbauer, E. Schäfer, Light induces rapid changes of the phosphorylation pattern in cytosol of evacuolated parsley protoplasts, Proc. Natl. Acad. Sci. USA, 1994, 91, 5038–5042.
J. Sheen, Protein phosphatase activity is required for light-inducible gene expression in maize, EMBO J., 1993, 12, 3497–3505.
M. R. Chandok and S. K. Sopory, Phosphorylation/dephosphorylation steps are key events in the phytochrome-mediated enhancement of nitrate reductase mRNA levels and enzyme activity in maize, Mol. Gen. Genet., 1996, 251, 599–608.
P. Malec, A. Yahalom and D. A. Chamovitz, Identification of a light-regulated protein kinase activity from seedlings of Arabidopsis thaliana, Photochem. Photobiol., 2002, 75, 178–183.
P. H. Quail, W. R. Briggs and L. H. Pratt, In vivo phosphorylation of phytochrome, Carnegie Institution Yearbook, 1978, 77, 342–344.
M. Ahmad, J. A. Jarillo, O. Smirnova and A. R. Cashmore, The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro, Mol. Cell, 1998, 1, 939–948.
D. Shalitin, H. Yang, T. C. Mockler, M. Maymon, H. Guo, G. C. Whitelam and C. Lin, Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation, Nature, 2002, 417, 763–767.
K.-C. Yeh and J. C. Lagarias, Eukaryotic phytochromes: Light-regulated serine/threonine protein kinases with histidine kinase ancestry, Proc. Natl. Acad. Sci. USA, 1998, 95, 13976–13981.
J. M. Christie, P. Reymond, G. K. Powell, P. Bernasconi, A. A. Raibekas, E. Liscum and W. R. Briggs, Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism, Science, 1998, 282, 1698–701.
J. P. Bouly, B. Giovani, A. Djamei, M. Mueller, A. Zeugner, E. A. Dudkin, A. Batschauer and M. Ahmad, Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1, Eur. J. Biochem., 2003, 270, 2921–2928.
D. Shalitin, X. Yu, M. Maymon, T. Mockler and C. Lin, Blue light-dependent in vivo and in vitro phosphorylation of Arabidopsis cryptochrome 1, Plant Cell, 2003, 15, 2421–2429.
C.-M. Park, S.-H. Bhoo, P.-S. Song, Inter-domain crosstalk in the phytochrome molecules, Sem. Cell Dev. Biol., 2000, 11, 449–456.
J.-I. Kim, G. V. Kozhukh, P.-S. Song, Phytochrome-mediated signal transduction pathways in plants, Biochem. Biophys. Res. Commun., 2002, 298, 457–463.
H. Wang, X.-W. Deng, Dissecting the phytochrome A-dependent signaling network in higher plants, Trends Plant Sci., 2003, 8, 172–178.
E. Schäfer and C. Bowler, Phytochrome-mediated photoperception and signal transduction in higher plants, EMBO Rep., 2002, 3, 1042–1048.
U. Sweere, K. Eichenberg, J. Lohrmann, V. Mira-Rodado, I. Baurle, J. Kudla, F. Nagy, E. Schäfer and K. Harter, Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling, Science, 2001, 294, 1108–1111.
Y. Zhu, J. M. Tepperman, C. D. Fairchild and P. H. Quail, Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix-loop-helix factor PIF3 in a reaction requiring the PAS domain of PIF3, Proc. Natl. Acad. Sci. USA, 2000, 97, 13419–13424.
B. L. Montgomery and J. C. Lagarias, Phytochrome ancestry: sensors of bilins and light, Trends Plant Sci., 2002, 7, 357–366.
J. R. Cherry, D. Hondred, J. M. Walker and R. D. Viestra, Phytochrome requires the 6-kDa N-terminal domain for full biological activity, Proc. Natl. Acad. Sci. USA, 1992, 89, 5039–5043.
E. T. Jordan, J. M. Marita, R. C. Clough and R. D. Viestra, Characterization of regions within the N-terminal 6-kilodalton domain of phytochrome A that modulate its biological activity, Plant Physiol., 1997, 115, 693–704.
J. J. Casal, S. J. Davis, D Kirchenbauer, A. Viczian, M. J. Yanovsky, R. C. Clough, S. Kircher, E. T. Jordan-Beebe, E. Schäfer, F. Nagy and R. D. Vierstra, The serine-rich N-terminal domain of oat phytochrome A helps regulate light responses and subnuclear localization of the photoreceptor, Plant Physiol., 2002, 129, 1127–1137.
D. Wagner, C. D. Fairchild, R. M. Kuhn and P. H. Quail, Chromophore-bearing NH2-terminal domains of phytochromes A and B determine their photosensory specificity and differential light lability, Proc. Natl. Acad. Sci. USA, 1996, 93, 4011–4015.
Y. Oka, T. Matsushita, N. Mochizuki, T. Suzuki, S. Tokutomi and A. Nagatani, Functional analysis of a 450-amino acid N-terminal fragment of phytochrome B in Arabidopsis, Plant Cell, 2004, 16, 2104–2116.
L. Krall and J. W. Reed, The histidine kinase-related domain participates in phytochrome B function but is dispensable, Proc. Natl. Acad. Sci. USA, 2000, 97, 8169–8174.
P. H. Quail, The phytochromes: a biochemical mechanism of signaling in sight?, BioEssays, 1997, 19, 571–579.
J.-I. Kim and P.-S. Song, unpublished.
C. Fankhauser, K. C. Yeh, J.-C. Lagarias, H. Zhang, T. D. Elich and J. Chory, PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis, Science, 1999, 284, 1539–1541.
T. Matsushita, N. Mochizuki and A. Nagatani, Dimers of the N-terminal domain of phytochrome B are functional in the nucleus, Nature, 2003, 424, 571–574.
Y.-S. Wong, H.-C. Cheng, D. A. Walsh and J. C. Clark, Phosphorylation of Avena phytochrome in vitro as a probe of light-induced conformational changes, J. Biol. Chem., 1986, 261, 12089–12097.
B. J. Biermann, L. I. Pao and L. J. Feldman, Pr specific phytochrome phosphorylation in vitro by a protein kinase present in anti-phytochrome maize immunoprecipitates, Plant Physiol., 1994, 105, 243–251.
R. W. McMichael, Jr. and J. C. Lagarias, Phosphopeptide mapping of Avena phytochrome phosphorylated by protein kinase in vitro, Biochemistry, 1990, 29, 3872–3878.
V. N. Lapko, X. Y. Jiang, D. L. Smith, P.-S. Song, Post-translational modification of oat phytochrome A: Phosphorylation of a specific serine in a multiple serine cluster, Biochemistry, 1997, 36, 10595–10599.
V. N. Lapko, X. Y. Jiang, D. L. Smith, P.-S. Song, Mass spectrometric characterization of oat phytochrome A: Isoforms and posttranslational modifications, Protein Sci., 1999, 8, 1032–1044.
V. N. Lapko, T. A. Wells, P.-S. Song, Protein kinase A-catalyzed phosphorylation and conformational changes in phytochrome A, Biochemistry, 1996, 35, 6585–6594.
C. Fankhauser, Phytochromes as light-modulated protein kinases, Semin. Cell Dev. Biol., 2000, 11, 467–473.
J. Stockhaus, A. Nagatani, U. Halfter, S. Kay, M. Furuya, N.-H. Chua, Serine-to-alanine substitutions at the amino-terminal region of phytochrome A result in an increase in biological activity, Genes Dev., 1992, 6, 2364–2372.
J.-I. Kim, Y. Shen, Y.-J. Han, D. Kirchenbauer, J.-E. Park, M.-S. Soh, F. Nagy, E. Schäfer, P.-S Song, Phytochrome phosphorylation modulates light signaling by influencing the protein–protein interaction, Plant Cell, 2004, 16, 2629–2640.
G. Choi, H. Yi, Y.-K. Kwon, M.-S. Soh, B. Shin, Z. Luka, T.-R. Hahn, P.-S. Song, Phytochrome signaling is mediated through nucleoside diphosphate kinase 2, Nature, 1999, 401, 610–613.
Y.-J. Im, J.-I. Kim, Y. Shen, Y. Na, Y.-J. Han, S.-H. Kim, P.-S. Song and S. H. Eom, Structural analysis of Arabidopsis thaliana nucleoside diphosphate kinase-2 for plant phytochrome signaling, J. Mol. Biol., 2004, 343, 659–670.
M. Ni, J. M. Tepperman and P. H. Quail, PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein, Cell, 1998, 95, 657–667.
E. Monte, J. M. Tepperman, B. Al-Sady, K. A. Kaczorowski, J. M. Alonso, J. R. Ecker, X. Li, Y. Zhang and P. H. Quail, The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development, Proc. Natl. Acad. Sci. USA., 2004, 101, 16091–16098.
Y.-S. Wong, R. W. McMichael, Jr. and J. C. Clark, Properties of a polycation-stimulated protein kinase associated with purified Avena phytochrome, Plant Physiol., 1989, 91, 709–718
H. A. W. Schneider-Poetsch, B. Braun, S. Marx and A. Schaumburg, Phytochromes and bacterial sensor proteins are related by structural and functional homologs/hypothesis on phytochrome-mediated signal transduction, FEBS Lett., 1991, 281, 245–259.
F. Thümmler, P. Algarra and G. M. Fobo, Sequence similarities of phytochrome to protein kinases: implication for the structure, function and evolution of the phytochrome gene family, FEBS Lett., 1995, 357, 149–155.
M. T. Boylan and P. H. Quail, Are the phytochromes protein kinases?, Protoplasma, 1996, 195, 12–17.
J. Hughes, T. Lamparter, F. Mittman, E. Hartmann, W. Gartner, A. Wilde and T. Boerner, A prokaryotic phytochrome, Nature, 1997, 386, 663.
K.-C. Yeh, S.-H. Wu, J. T. Murphy and J. C. Lagarias, A cyanobacterial phytochrome two-component light sensory system, Science, 1997, 277, 1505–1508.
A. Colón-Carmona, D. L. Chen, K.-C. Yeh and S. Abel, Aux/IAA proteins are phosphorylated by phytochrome in vitro, Plant Physiol, 2000, 124, 1728–1738.
S.-H. Bhoo, S. J. Davis, J. Walker, B. Karniol and R. D. Vierstra, Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore, Nature, 2001, 414, 776–779.
V. N. Lapko and P.-S. Song, unpublished.
I.-S. Kim and J.-I. Kim, unpublished.
F. Thümmler, R. Herbst, P. Algarra and A. Ullrich, Analysis of the protein kinase activity of moss phytochrome expressed in fibroblast cell culture, Planta, 1995, 197, 592–596.
D.-H. Kim, J.-G. Kang, S.-S. Yang, K.-S. Chung, P.-S. Song, C.-M. Park, A phytochrome associated protein phosphatase 2A modulates light signals in flowering time control in Arabidopsis, Plant Cell, 2002, 14, 3043–3056.
J. S. Ryu, J.-I. Kim, T. Kunkel, B. C. Kim, D. S. Cho, S. H. Hong, S.-H. Kim, A. P. Fernández, Y. Kim, J. M. Alonso, J. R. Ecker, F. Nagy, P. O. Lim, P.-S. Song, E. Schäfer and H. G. Nam, Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal trasducer, Cell, 2005, 120, 395–406.
S. G. Møller, Y.-S. Kim, T. Kunkel, N.-H. Chua, PP7 is a positive regulator of blue light signaling in Arabidopsis, Plant Cell, 2003, 15, 1111–1119.
I. Sokal, A. Pulvermuller, J. Buczylko, K. P. Hofmann and K. Palczawski, Rhodopsin and its kinase, Methods Enzymol., 2002, 343, 578–600.
J.-I. Kim and P.-S. Song, unpublished.
V. Y. Arshavsky, Rhodopsin phosphorylation: from terminating single photon responses to photoreceptor dark adaptation, Trends Neurosci., 2002, 25, 124–126.
J. M. Maloof, J. O. Borevitz, T. Dabi, J. Lutes, R. B. Nehring, J. L. Redfern, G. T. Trainer, J. M. Wilson, T. Asami, C. C. Berry, D. Weigel and J. Chory, Natural variation in light sensitivity of Arabidopsis, Nature Genetics, 2001, 29, 441–446.
P. Lariguet, H. E. Boccalandro, J. M. Alonso, J. R. Ecker, J. Chory, J. J. Casal and C. Fankhauser, A growth regulatory loop that provides homeostasis to phytochrome a signaling, Plant Cell, 2003, 15, 2966–2978.
H. Hellmann and M. Estelle, Plant development: Regulation by protein degradation, Science, 2002, 297, 793–797.
J.-G. Kang, J. Yun, D.-H. Kim, K.-S. Chung, S. Fujioka, J.-I. Kim, H.-W. Dae, S. Yoshida, S. Takatsuti, P.-S. Song, C.-M. Park, Light and brassinosteroid signals are integrated via a dark-induced small G protein in etiolated seedling growth, Cell, 2001, 105, 625–636.
F. Nagy, E. Schäfer, Phytochrome control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants, Annu. Rev. Plant Biol., 2002, 53, 329–355.
S. Kircher, P. Gil, L. Kozma-Bognar, E. Fejes, V. Speth, T. Husselstein-Muller, D. Bauer, E. Adam, E. Schafer and F. Nagy, Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm, Plant Cell, 2002, 14, 1541–1555.
R. A. Sharrock and T. Clack, Patterns of expression and normalized levels of the five Arabidopsis phytochromes, Plant Physiol., 2002, 130, 442–456.
A. C. Mustilli and C. Bowler, Tuning in to the signals controlling photoregulated gene expression in plants, EMBO J., 1997, 16, 5801–5806.
H. Guo, T. Mockler, H. Duong and C. Lin, SUB1, an Arabidopsis Ca2+-binding protein involved in cryptochrome and phytochrome coaction, Science, 2001, 291, 487–490.
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Presented at the 14th International Congress on Photobiology, at Jungmoon, Jeju Island, South Korea, 10th-15th June 2004.
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Kim, JI., Park, JE., Zarate, X. et al. Phytochrome phosphorylation in plant light signaling. Photochem Photobiol Sci 4, 681–687 (2005). https://doi.org/10.1039/b417912a
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DOI: https://doi.org/10.1039/b417912a