Transduction mechanisms of photoreceptor signals in plant cells

Journal of Photochemistry and Photobiology C: Photochemistry Reviews

Volumn 10, Issue 2, 2009, Pages 63-80

  Kreslavski, Vladimir D ^a   Carpentier, Robert ^b   Klimov, Vyacheslav V ^a   Allakhverdiev, Suleyman I ^a  

^a INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

^b UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

Ion exchange; Photoreceptors; Phytochrome; Plant; Signal transduction; Transcriptional factors

Indexed keywords

A PLANTS; HIGHER PLANTS; IN-PLANT; INFORMATION SIGNALS; ION EXCHANGE SYSTEMS; LIGHT-SIGNAL TRANSDUCTION; PHOTORECEPTORS; PHYTOCHROME; PLANT; PLANT METABOLISM; REGULATORY FACTORS; SIGNALING EVENTS; SIGNALING PATHWAYS; SOURCE OF ENERGY; TRANSCRIPTIONAL FACTORS; TRANSDUCTION MECHANISM;

BACTERIOPHAGES; ION EXCHANGE; ION EXCHANGERS; IONS; SIGNALING;

SIGNAL TRANSDUCTION;

EID: 67651175855     PISSN: 13895567     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotochemrev.2009.04.001     Document Type: Review

References (197)

1. Neuhaus G., Bowler C., Kern R., and Chua N.-H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73 (1993) 937-952
2. Neff M.M., Fankhauser C., and Chory J. Light: an indicator of time and place. Genes Dev. 14 (2000) 257-271
3. Schäfer E., and Bowler C. Phytochrome-mediated photoreception and signal transduction in higher plants. EMBO Reports 3 (2002) 1042-1048
4. Wang H., and Deng X.W. Phytochrome Signaling Mechanism. The Arabidopsis Book (2002), American Society of Plant Biologists p. 238
5. Lin C. Blue light receptors and signal transduction. Plant Cell 14 (2002) 207-225
6. Wang H., and Deng X.W. Dissecting the phytochrome A-dependent signaling network in higher plants. Trends Plant Sci. 4 (2003) 172-178
7. Nayyar H. Calcium as environmental sensor in plants. Curr. Sci. 84 (2003) 893-902
8. Chen M., Chory J., and Fankhauser C. Light signal transduction in higher plants. Ann. Rev. Gen. 38 (2004) 87-117
9. Spalding E.P., and Folta K.M. Illuminating topics in plant photobiology. Plant Cell Environ. 28 (2005) 39-53
10. Medvedev S.S. Plant calcium signaling system. Russ. J. Plant Physiol. 52 (2005) 282-305
11. Kreslavski V.D., and Allakhverdiev S.I. Transduction mechanisms of photoreceptor signal in plant cell. Russ. J. Biologicheskie Membrany 23 (2006) 275-295
12. Schäfer E., and Nagy F. Photomorphogenesis in Plants and Bacteria. Function and Signal Transduction Mechanisms (2006), Springer, Dordrecht, The Netherlands
13. Jiao Y., Lau O.S., and Deng X.W. Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 8 (2007) 217-230
14. Beato M., Chavez S., and Truss M. Transcriptional regulation by steroid hormones. Steroids 61 (1996) 240-251
15. 3 and cyclic ADP-ribose. Science 268 (1995) 735-737
16. Sopory S.K., and Chandok M.R. Light induced signal transduction pathway involving inositol phosphates. Sub. Cell Biochem. 26 (1996) 345-370
17. Sanders D., Colin B., and Harper J.F. Communicating with calcium. Plant Cell 11 (1999) 691-706
18. Sanders D., Pelloux J., Brownlee C., and Harper J.F. Calcium at the crossroads of signaling. Plant Cell 14 (2002) 401-417
19. Trewavas A.J., Rodrigues C., Rato C., and Malho R. Cyclic nucleotides: the current dilemma. Curr. Opin. Plant Biol. 5 (2002) 425-429
20. Yang W., and Xia S. Mechanisms of regulation and function of G-protein-coupled receptor kinases. World J. Gastroenterol. 12 (2006) 7753-7757
21. Bowler C., Neuhaus G., Yamagata H., and Chua N.-H. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77 (1994) 73-81
22. 2+ and intracellular signaling in plant cells: a role in phytochrome transduction. Membr. Cell Biol. 12 (1998) 721-742
23. Volotovski I.D., Sokolovsky S.G., Molchan O.V., and Knight M.R. Second messengers mediate increases in cytosolic calcium in tobacco protoplasts. Plant Physiol. 117 (1998) 1023-1030
24. Okamoto H., Matsui M., and Deng X.W. Overexpression of the heterotrimeric G-protein α-subunit enhances phytochrome-mediated inhibition of hypocotyl elongation in Arabidopsis. Plant Cell 13 (2001) 1639-1652
25. Assmann S.M. Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 14 (2002) 355-373
26. Hurvey J.H. The adenylyl and guanylyl cyclase superfamily. Curr. Opin. Struct. Biol. 8 (1998) 770-777
27. Maheshwari S.C., Khurana J.P., and Sopory S.K. Novel light-activated protein kinases as key regulators of plant growth and development. Biosciences 24 (1999) 499-514
28. Roux S.J. Signal transduction in phytochrome responses. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Higher Plants. 2nd ed. (1994), Kluwer Academic Publishers, Dordrecht 187-209
29. Ni M., Tepperman J.M., and Quail P.H. PIF3, a phytochrome interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95 (1998) 657-667
30. Ni M., Tepperman J.M., and Quail P.H. Binding of phytochrome B to its nuclear signaling partner PIF3 is reversibly induced by light. Nature 400 (1999) 781-784
31. Christie J.M., and Briggs W.R. Blue light sensing in higher plants. J. Biol. Chem. 276 (2001) 11457-11460
32. Al-Sady B., Ni W., Kircher S., Schäfer E., and Quail P.H. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23 (2006) 439-446
33. Nagy F., and Schäfer E. Nuclear and cytosolic events of light-induced, phytochrome-regulated signaling in higher plants. EMBO J. 19 (2000) 157-163
34. Huq E., and Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21 (2002) 2441-2450
35. Oh E., Kim J., Park E., Kim J.-I., Kang C., and Choi G. PIL5, phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16 (2004) 3045-3058
36. Quail P.H. Phytochrome signal transduction network. In: Schäfer E., and Nagy F. (Eds). Photomorphogenesis in Plants and Bacteria (2006), Springer, Dordrecht, The Netherlands 335-356
37. Osterlund M.T., Hardtke C.S., Wei N., and Deng X.W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405 (2000) 462-466
38. Bowler C., and Chua N.-H. Emerging themes of plant signal transduction. Plant Cell 6 (1994) 1529-1541
39. Kendrick R.E., and Kronenberg G. In: Kendric R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands
40. Quail P.H. Phytochrome photosensory signaling networks. Nat. Rev. Mol. Cell Biol. 3 (2002) 85-93
41. Briggs W.R., and Olney M.A. Photoreceptors in plant photomorphogenesis to date: five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol. 125 1 (2001) 85-88
42. Folta K.M. Green light stimulates early stem elongation, antagonizing light-mediated growth inhibition. Plant Physiol. 135 (2004) 1407-1416
43. Tokutomi S., Matsuoka D., and Zikihara K. Molecular structure and regulation of phototropin kinase by blue light. Biochim. Biophys. Acta 1784 (2008) 133-142
44. Rockwell N.C., Su Y.-S., and Lagarias J.C. Phytochrome structure and signaling mechanisms. Ann. Rev. Plant Biol. 57 (2006) 837-858
45. Krall L., and Reed J.W. The histidine kinase-related domain participates in phytochrome B function but is dispensable. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 8169-8174
46. Sharrock R.A., and Clack T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 130 (2002) 442-456
47. Tu S.L., and Lagarias J.C. The phytochromes. In: Briggs W.R., and Spudich J. (Eds). Handbook of Photosensory Receptors (2005), Wiley-VCH, Weinheim, Germany 121-145
48. Møller S.G., Ingles P.J., and Whitelam G.C. The cell biology of phytochrome signaling. New Physiol. 154 (2002) 553-590
49. Mancinelli A.L. The physiology of phytochrome action. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands 211-269
50. Smith H. Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407 (2000) 585-691
51. Ma L.-G., Li J.-M., Qu L.-J., Chen Z.-L., Zhao H.-Y., and Deng X.W. Light control of Arabidopsis development entails co-ordinated regulation of genome expression and cellular pathways. Plant Cell 13 (2001) 2589-2607
52. Hughes J., Lamparter T., Mittmann F., Hartmann E., Gärtner W., Wilde A., and Börner T. A prokaryotic phytochrome. Nature 386 (1997) 663
53. Bhoo S.-H., Davis S.J., Walker J., Karniol B., and Vierstra R.D. Bacteriophytochromes are photochromic histidine kinase using a biliverdin chromophore. Nature 414 (2001) 776-777
54. Lamparter T., and Hughes J. Phytochromes and phytochrome-like proteins in cyanobacteria. In: Batschauer A. (Ed). Photoreceptors and Light Signalling (2003), Cambridge, RSC, UK 203-227
55. Mutsuda M., Michel K.P., Zhang X.F., Montgomery B.L., and Golden S.S. Biochemical properties of CikA, an unusual phytochrome-like histidine protein kinase that resets the circadian clock in Synechococcus elongatus PCC7942. J. Biol. Chem. 278 (2003) 19102-19110
56. Evans K., Fordham-Skelton A.P., Mistry H., Reynolds C.D., Lawless A.M., and Papiz M.Z. A bacteriophytochrome regulates the synthesis of LH4 complexes in Rhodopseudomonas palustris. Photosynth. Res. 85 (2005) 169-180
57. Fankhauser C., Yeh K.C., Lagarias J.C., Zhang H., Elich T.D., and Chory J. PKS1, a substrate phosphorylated by phytochromes that modulates light signaling in Arabidopsis. Science 284 (1999) 1539-1541
58. Lin C., and Shalitin D. Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54 (2003) 469-496
59. Briggs W.R., and Christie J.M. Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7 (2002) 204-210
60. Christie J.M. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58 (2007) 21-45
61. Imaizumi T., Tran H.G., Swartz T.E., Briggs W.R., and Kay S.A. FKF1 is essential for photoperiodic-specific light signaling in Arabidopsis. Nature 426 (2003) 302-306
62. Brown B.A., Cloix C., Jiang G.H., Kaiserli E., Herzyk P., Kliebenstein D.J., and Jenkins G.I. A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102 50 (2005) 18225-18230
63. Nozue K., Kanegae T., Imaizumi T., Fukuda S., Okamoto H., Yeh K.C., Lagarias J.C., and Wada M. A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 15826-15830
64. Kawai H., Kanegae T., Christensen S., Kiyosue T., Sato Y., Imaizumi T., Kadota A., and Wada M. Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421 (2003) 287-290
65. Suetsugu N., Mittmann F., Wagner G., Hughes J., and Wada M. A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 13705-13709
66. Borthwick H.A., Hendricks S.B., Parker M.W., Toole E.H., and Toole V.K. A reversible photoreaction controlling seed germination. Proc. Natl. Acad. Sci. U.S.A. 38 (1952) 662-666
67. Wagner G. Cryptochrome, phototropin and phytochrome: molecules, evolution and interaction. In: Volotovski I.D. (Ed). Plant Photobiology and Photosynthesis (2000), Natl. Acad. Sci. Belarus, Minsk 55-123
68. Kobzar' E.F., Kreslavski V.D., and Muzafarov E.N. Red radiation and choline compounds influence growth and greening of wheat seedlings. Photosynthetica 36 (1999) 333-340
69. Kreslavski V.D., Kobzar' E.F., and Muzafarov E.N. Effect of red light and linuron on growth and ethylene production in Chlorella. Biol. Plant 39 (1997) 427-430
70. Koornneef M., Cone J.W., Dekens R.G., O'Herne-Roberts E.G., Spruit C.J.P., and Kendrick R.E. Photomorphogenic responses of long hypocotyl mutants of tomato. J. Plant Physiol. 120 (1985) 153-165
71. Haupt W., and Häder D.P. Photomovement. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Higher Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands 707-732
72. Kraml M. Light direction and polarisation. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Higher Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands 186-191
73. Pratt L.H. Distribution and localization of phytochrome within the plant. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Higher Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands 163-185
74. Kircher S., Gil P., Kozma-Bognar L., Fejes E., Speth V., Husselstein-Muller T., Bauer D., Adam E., Schäfer E., and Nagy F. 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 14 (2002) 1541-1555
75. Haupt W. Light-mediated movement of chloroplasts. Annu. Rev. Plant Physiol. 33 (1982) 205-233
76. Winands A., and Wagner G. Phytochrome of green alga Mougeotia: cDNA sequence, autoregulation and phylogenetic position. Plant Mol. Biol. 32 (1996) 589-597
77. Mittmann F., Brücker G., Zeidler M., Repp A., Abts T., Hartmann E., and Hughes J. Targeted knockout in Physcomitrella reveals direct actions of phytochrome in the cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13939-13944
78. Kircher S., Kozma-Bognar L., Kim L., Adam E., Harter K., Schäfer E., and Nagy F. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11 (1999) 1445-1456
79. Kim L., Kircher S., Toth R., Adam E., Schäfer E., and Nagy F. Light induced nuclear import of phytochrome-A:GFP fusion proteins is differentially regulated in transgenic tobacco and Arabidopsis. Plant J. 22 (2000) 125-133
80. Yamaguchi R., Nakamura M., Mochizuki N., Kay S.A., and Nagatani A. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J. Cell Biol. 145 (1999) 437-445
81. Kim J., Yi H., Choi G., Shin B., Song P.-S., and Choi G. Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15 (2003) 2399-2407
82. Whitelam G.C., and Devlin P.F. Distribution and localization of phytochrome within the plant. Plant Cell Environ. 20 (1997) 752-758
83. Smith H., and Whitelam G.C. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20 (1997) 840-844
84. Kircher S., Wellmer F., Nick P., Rügner A., Schäfer E., and Harter K. Nuclear import of the parsley bZIP transcription factor CPRF2 is regulated by phytochrome photoreceptors. J. Cell Biol. 144 (1999) 201-211
85. Wellmer F., Kircher S., Rügner A., Frohnmeyer H., Schäfer E., and Harter K. Phosphorylation of the parsley bZIP transcription factor CPRF2 is regulated by light. J. Biol. Chem. 274 (1999) pp. 29476-19482
86. Chung C.H., Lim S.-V., Song P.-S., Berlin J.D., and Gooding J.R. Swelling of etiolated oat protoplasts induced by phytochrome, cAMP, and gibberellic acid: a kinetic study. Plant Cell Physiol. 29 (1988) 855-860
87. 2+-dependent swelling of etiolated wheat protoplasts. Physiol. Plant 80 (1990) 55-62
88. Shacklock P.S., Read N.D., and Trewavas A.J. Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358 (1992) 753-755
89. + channels and chloroplast rotation in Mougeotia: the escape times. Plant Cell Physiol. 37 (1996) 175-179
90. Johannes E., Ermolayeva E., and Sanders D. Red light-induced membrane potential transients in the moss Physcomitrella patens: ion channel interaction in phytochrome signaling. J. Exp. Bot. 48 (1997) 599-608
91. Roelfsema M.R.G., and Hedrich R. Studying guard cells in the intact plant: modulation of stomatal movement by apoplastic factors. New Physiol. 153 (2002) 425-431
92. Takagi S., Kong S.G., Mineyuki Y., and Furuya M. Regulation of actin-dependent cytoplasmic motility by type II phytochrome occurs within seconds in Vallisneria gigantea epidermal cells. Plant Cell 15 (2003) 331-345
93. 2+ through different manners in Arabidopsis leaves. Proc. Natl. Acad. Sci. U.S.A. 14 (2003) 8583-8588
94. Racusen R., and Satter R.L. Rhythmic and phytochrome-regulated changes in transmembrane potential in Samanea pulvini. Nature 255 (1975) 408-410
95. Spalding E.P. Ion channels and the transduction of light signals. Plant Cell Environ. 23 (2000) 665-674
96. Aidley D.J., and Stanfield P.R. Ion Channels: Molecules in Action (1996), Cambridge University Press, Cambridge, New York pp. 204
97. Zimmermann S., Ehrhardt T., Plesch G., and Müller-Röber B. Ion channels in plant signaling. Cell. Mol. Life Sci. 55 (1999) 183-203
98. White P.J. Calcium channels in higher plants. Biochim. Biophys. Acta 1465 (2000) 171-189
99. Nagata T., Iizumi S., Satoh K., Ooka H., Kaway J., Carninci P., Hayashizaki Y., Otomo Y., Murakami K., Matsubara K., and Kikuchi S. Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol. Biol. Evol. 21 (2004) 1855-1870
100. Spalding E.P., and Cosgrove D.J. Large plasma-membrane depolarization precedes rapid blue-light-induced growth inhibition in cucumber. Planta 178 (1989) 407-410
101. Cho M.H., and Spalding E.P. An anion channel in Arabidopsis hypocotyls activated by blue light. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 8134-8138
102. Ermolayeva E.D., Sanders S., and Johannes E. Ionic mechanism and role of phytochrome-mediated membrane depolarization in caulonemal side branch initial formation in the moss Physcomitrella patens. Planta 201 (1997) 109-118
103. 2+ channels in isolated red beet root vacuole membrane by inositol 1,4,5-trisphosphate. Nature 343 (1990) 567-570
104. Lemtiri-Chlieh F., and Berkowitz G.A. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J. Biol. Chem. 279 34 (2004) 35306-35312
105. 2+-channels in Nitelopsis optusa, Characeae cell plasmalemma and regulation of their activity. Comp. Biochem. Physiol. 94A 1 (1989) 141-145
106. Demidchik V., Davenport R.J., and Tester M. Nonselective cation channels in plants. Annu. Rev. Plant Biol. 53 (2002) 67-107
107. Roux S.J., and Yguerabide J. Photoreversible conductance changes induced by phytochrome in model lipid membranes. Proc. Natl. Acad. Sci. U.S.A. 70 3 (1973) 762-764
108. Weisenseel M.N., and Ruppert H.K. Phytochrome and calcium iones are involved in light-induced membrane depolarization in Nitella. Planta 137 (1977) 225-229
109. Böse G., Schwille P., and Lamparter T. The mobility of phytochrome within protonemal tip cells of the moss Ceratodon purpureus, monitored by fluorescence correlation spectroscopy. Biophys. J. 87 (2004) 2013-2021
110. Yeh K.C., and Lagarias J.C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13976-13981
111. Fankhauser C. Phytochromes as light-modulated protein kinases. Cell Dev. Biol. 11 (2001) 467-473
112. Mäser P., Thomine S., Schroeder J.I., Ward J.M., Hirschi K., et al. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126 (2001) 1646-1667
113. Lew R.R., Serlin B.S., Schaut C.L., and Stockton M.E. Red light regulates calcium-activated potassium channels in Mougeotia plasma membrane. Plant Physiol. 92 (1990) 822-830
114. + channels in the plasmalemma of Eremosphaera viridis. FEBS Lett. 269 (1990) 197-201
115. 2+ channels and signaling in higher plants. J. Exp. Bot. 48 (1997) 589-597
116. Kohler C., Merkle T., and Neuhaus G. Characterization of a novel gene family of putative cyclic nucleotide and calmodulin-regulated ion channels in Arabidopsis thaliana. Plant J. 18 (1999) 97-104
117. Kohler C., and Neuhaus G. Characterization of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. FEBS Lett. 471 (2000) 133-136
118. Aoyama T., and Chua N.-H. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11 (1997) 605-612
119. 2+-channel by TG α1, a heterotrimeric G-protein α-subunit homologue. FEBS Lett. 424 (1998) 17-21
120. Jones A.M., Ecker J.R., and Chen J.-G. A reevaluation of the role of the heterotrimeric G protein in coupling light responses in Arabidopsis. Plant Physiol. 131 (2003) 1623-1627
121. Nishizuka Y. Protein kinase signal transduction. Trends Biochem. Sci. 9 4 (1984) 163-166
122. Kostyuk P.G., and Ostrovskaya M.A. Intracellular Signalling (1988), Nauka, Moscow (in Russian)
123. Thion L., Mazars C., Thuleau P., Graziana A., Rossignol M., Moreau M., and Ranjeva R. Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of microtubules in carrot cells. FEBS Lett. 340 (1996) 45-50
124. Tretyn A., Kendrick R.E., and Bossen M.E. The effect of a calcium-channel antagonist, nifedipine and agonist Bay K-8644, on the phytochrome-controlled swelling of etiolated wheat protoplasts. Physiol. Plant 78 (1990) 230-235
125. Neuhaus G., Bowler C., Hiratsuka K., Yamagata H., and Chua N.-H. Phytochrome-regulated repression of gene expression requires calcium and cGMP. EMBO J. 16 (1997) 2554-2564
126. 2+-ionophore A23187 and by calmodulin antagonists. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 6368-6372
127. Elzenga J., Staal M., and Prins H. Calcium-calmodulin signaling is involved in light-induced acidification by epidermal leaf cells of pea, Pisum sativum L. J. Exp. Bot. 48 (1997) 2055-2060
128. Wang X., and Iino M. Interaction of cryptochrome 1, phytochrome, and ion fluxes in blue- light-induced shrinking of Arabidopsis hypocotyl protoplasts. Plant Physiol. 117 (1998) 1265-1279
129. 2+ in the green alga Mougeotia scalaris as monitored with indo-1, and their effect on the velocity of chloroplast movement. Planta 184 (1991) 105-112
130. Knight M.R., Knight H., and Watkins N.J. Calcium and the generation of plant form. Philos. Trans. R. Soc. Lond. (B) 350 (1995) 83-86
131. Volotovski I.D. Transduction mechanisms of plant phytochrome effects. Russ. J. Biophys. 40 4 (1995) 1291-1307
132. Berridge M.J., Bootman M.D., and Roderick H.L. Calcium signalling: dynamics, homeostasis and remodeling. Nat. Rev. Mol. Cell Biol. 4 (2003) 517-529
133. Thaler M., Steigner W., Förster B., Köhler K., Simonis W., and Urbach W. Calcium activation of potassium channels in the plasmalemma of Eremosphaera viridis. J. Exp. Bot. 40 (1989) 1195-1203
134. Zielinski R.E. Calmodulin and calmodulin binding protein in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 3 (1998) 697-725
135. Reddy V.S., Ali G.S., and Reddy A.S. Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J. Biol. Chem. 277 (2002) 9840-9852
136. Zörb C., Brunner K.D., Perbandt M., Betzel Ch., and Wagner G. Cloning, recombinant expression and characterization of wild type-105-trp-calmodulin of the green alga Mougeotia scalaris. Bot. Acta 111 (1998) 346-353
137. 2+/calmodulin-dependent protein kinase cascades in transcriptional regulation. J. Biol. Chem. 276 5 (2001) 2975-2978
138. Mueller-Roeber B., and Pical C. Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol. 130 (2002) 22-46
139. Newton R.P., Roef L., Witters E., and Van Onckelen H. Cyclic nucleotides in higher plants: the enduring paradox. New Phytol. 143 (1999) 427-455
140. Richards H., Das S., Smith C.H., Pereira L., Geisbrecht A., Devitt N.J., Games D.E., van Geyschem J., Brenton A.G., and Newton R.P. Cyclic nucleotide content of tobacco BY-2 cells. Phytochemistry 61 5 (2002) 531-537
141. 2+ release across nonvacuolar membranes in cauliflower. Plant Physiol. 114 (1997) 1511-1521
142. Dubovskaya L.V., Molchan O.V., and Volotovski I.D. Photoregulation of endogenic level of cAMP in oat seedlings. Russ. J. Plant Physiol. 48 1 (2001) 26-29
143. Volotovski I.D., Dubovskaya L.V., and Molchan O.V. Photoreceptor phytochrome regulates the cyclic guanosine 3,5-monophosphate synthesis in Avena sativa L. cells. Bulg. J. Plant Physiol. 29 1-2 (2003) 3-12
144. Sopory S.K., and Munshi M. Protein kinases and phosphatases and their role in signalling in plants. Crit. Rev. Plant Sci. 17 (1998) 245-318
145. Zhang L., and Lu Y.-T. Calmodulin-binding protein kinases in plants. Trends Plant Sci. 8 (2003) 123-127
146. Pandey S., and Sopory S.K. Zea mays CCaMK: autophosphorylation-dependent substrate phosphorylation and down-regulation by red light. J. Exp. Bot. 52 357 (2001) 691-700
147. Elliott D.C., and Skinner J.D. Calcium-dependent phospholipids-activated protein kinase in plants. Photochemistry 25 1 (1986) 39-45
148. Elliott D.C., and Kokke V.S. Partial purification and properties of a protein kinase C type enzyme from plants. Photochemistry 26 (1987) 2929-2935
149. Janmey P.A. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol. Rev. 78 (1998) 763-781
150. Wagner G. Intracellular movement. Prog. Bot. 57 (1996) 68-80
151. Al-Rawass B., Grolig F., and Wagner G. High irradiance blue light affects cortical microtubules in the green alga Mougeotia scalaris. Plant Cell Physiol. 38 (1997) 882-886
152. Klyachko N.L. Actin cytosceleton and shape of plant cell. Russ. J. Plant Physiol. 51 6 (2004) 918-925
153. Quail P.H. Phytochrome interacting factors. In: Whitelam G., and Halliday K. (Eds). Light and Plant Development (2007), Blackwell Publishing, Oxford, UK 81-105
154. Choi G., Yi H., Lee J., Kwon Y.-K., Soh M.S., Shin B., Luka Z., Hahn T.R., and Song P.-S. Phytochrome signaling is mediated through nucleoside diphosphate kinase 2. Nature 401 (1999) 610-613
155. Tanaka N., Ogura T., Noguchi T., Hirano H., Yabe N., and Hasunuma K. Phytochrome-mediated light signals are transduced to nucleoside diphosphate kinase in Pisum sative L. cv. Alaska. J. Photochem. Photobiol. B 45 (1998) 113-121
156. Martinez-Garcia J.F., Huq E., and Quail P.H. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288 (2000) 859-863
157. Eckardt N.A. Light signaling revisited. Plant Cell 16 (2004) 1355-1357
158. Shen H., Moon J., and Huq E. PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44 (2005) 1023-1035
159. Shen Y., Khanna R., Christine M., Carle C.M., and Quail P.H. Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 145 (2007) 1043-1051
160. Shen Y., Kim J.-I., and Song P.-S. NDPK2 as a signal transducer in the phytochrome-mediated light signaling. J. Biol. Chem. 280 7 (2005) 5740-5749
161. Kim J., Shen Y., Han Y.J., Park J.E., Kirchenbauer D., Soh M.S., Nagy F., Schafer E., and Song P.S. Phytochrome phosphorylation modulates light signaling by influencing the protein-protein interaction. Plant Cell 16 (2004) 2629-2640
162. Chory J., and Wu D. Weaving the complex web of signal transduction. Plant Physiol. 125 (2001) 77-80
163. Mohr H. Coaction between pigment systems. In: Kendrick R.E., and Kronenberg G.H.M. (Eds). Photomorphogenesis in Plants (1994), Kluwer Academic Publishers, Dordrecht, The Netherlands 353-376
164. Casal J.J. Phytochromes, cyptochromes, phototrop, photoreceptor interactions in plants. Photochem. Photobiol. 71 (2000) 1-11
165. Lingakumar K., and Kulandaivelu G. Regulatory role of phytochrome on ultraviolet-B (280-315 nm) induced changes in growth and photosynthetic activity of Vigna sinensis L. Photosynthetica 29 3 (1993) 341-351
166. Kobzar' E.F., Kreslavski V.D., and Muzafarov E.N. Photomorphogenetic responses to UV radiation and short-term red light in lettuce seedlings. Plant Growth Regul. 26 (1998) 73-76
167. Eisinger W., Bogomolni R.A., and Taiz L. Interactions between a blue-green reversible photoreceptor and a separate UV-B receptor in stomatal guard cells. Am. J. Bot. 90 (2003) 1560-1566
168. Kreslavski V.D., Ivanov A.A., and Kosobrukhov A.A. Low energy light in the 620-660 nm range reduces the UV-B-induced damage to photosystem II in spinach leaves. Biophysics 49 5 (2004) 767-771
169. Surpin M., Larkin R.M., and Chory J. Signal transduction between the chloroplast and the nucleus. Plant Cell Supplement (2002) S327-338
170. Kropat J., Oster U., Rudiger W., and Beck C.F. Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14168-14172
171. Kropat J., Oster U., Rudiger W., and Beck C.F. Chloroplast signaling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to the cytoplasm/nucleus. Plant J. 24 (2000) 523-531
172. Susek R.E., Ausubel F.M., and Chory J. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74 (1993) 787-799
173. Møller S.G., Kunkel T., and Chua N.-H. A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev. 15 (2001) 90-103
174. Mochizuki N., Brusslan J.A., Larkin R., Nagatani A., and Chory J. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 2053-2058
175. Karu T. Mechanisms of low-power laser light action on cellular level. In: Simunovic Z. (Ed). Lasers in Medicine and Dentistry (2000), Vitgraf, Rijeka (Croatia) 97-125
176. Karu T.I. Mitochondrial signaling in mammalian cells activated by red and near-IR radiation. Photochem. Photobiol. 84 (2008) 1091-1099
177. Karu T.I., Pyatibrat L.V., and Afanasyeva N.I. A novel mitochondrial signaling pathway activated by visible-to-near infrared radiation. Photochem. Photobiol. 80 (2004) 366-372
178. Schroeder P., Pohl C., Calles C., Marks C., Wild S., and Krutmann J. Cellular response to infrared radiation involves retrograde mitochondrial signaling. Free Radic. Biol. Med. 43 (2007) 128-135
179. Karu T. Primary and secondary mechanisms of action of visible-to-near IR radiation on cells. J. Photochem. Photobiol. B. Biol. 49 (1999) 1-17
180. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 287 (2004) C817-C833
181. Ryan M.T., and Hoogenraad N.J. Mitochondrial-nuclear communications. Annu. Rev. Biochem. 76 (2007) 701-722
182. Ntefidou M., Iseki M., Watanabe M., Lebert M., and Häder D.-P. Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. Plant Physiol. 133 (2003) 1517-1521
183. Fabijan D.M., Dhindsa P.P., and Reid D.M. Effects of growth retardants on tissue permeability in Pisum sativum and Beta vulgaris. Planta 152 (1981) 481-486
184. Novitskaya G.V., Kocheshkova T.K., Feofitilactova T.V., and Novotski Yu.I. Effect of choline chloride on lipid content and composition in leaves of major magnetooriented redish species. Russ. J. Plant Physiol. 46 4 (2004) 618-625
185. Allakhverdiev S.I., Nishiyama Y., Suzuki I., Tassaka Y., and Murata N. Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5862-5867
186. Allakhverdiev S.I., Kinoshita M., Inaba M., Suzuki I., and Murata N. Unsaturated fatty acids in membrane lipids protect the photosynthestic machniary against salt-induced damage in Synechococcus. Plant Physiol. 125 (2001) 1842-1853
187. Allakhverdiev S.I., Sakamoto A., Nishiyama Y., and Murata N. Inactivation of photosystems I and II in response to osmotic stress in Synechococcus. Contribution of water channels. Plant Physiol. 122 (2000) 1201-1208
188. Allakhverdiev S.I., Sakamoto A., Nishiyama Y., Inaba M., and Murata N. Ionic and osmotic effects of NaCl-induced inactivation of photosystem I and II in Synechococcus. Plant Physiol. 123 (2000) 1047-1056
189. Allakhverdiev S.I., and Murata N. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta 1657 (2004) 23-32
190. Allakhverdiev S.I., and Murata N. Salt stress inhibits photosystems II and 1 in cyanobacteria. Photosynth. Res. 98 (2008) 529-539
191. Kanesaki Y., Suzuki I., Allakhverdiev S.I., Mikami K., and Murata N. Salt stress and hyperosmotic stress regulate the expression of different sets of genes in II in Synechocystis sp. PCC 6803. Biochem. Biophys. Res. Commun. 290 (2002) 339-348
192. Shapiguzov A., Lyukevich A.A., Allakhverdiev S.I., Sergeyenko T.V., Suzuki I., Murata N., and Los' D.A. Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates the osmostress-inducible gene expression. Microbiology 151 (2005) 447-455
193. Qi Z., Yue M., Han R., and Wang X.L. The damage repair role of He-Ne laser on plants exposed to different intensities of ultraviolet-B radiation. Photochem. Photobiol. 75 (2002) 680-686
194. Leivar P., Monte E., Al-Sady B., Carle C., Storer A., Alonso J.M., Ecker J.R., and Quail P.H. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20 (2008) 337-352
195. Casal J.J., and Yanovsky M.J. Regulation of gene expression by light. Int. J. Dev. Biol. 49 (2005) 501-511
196. Quail P.H. Phytochrome-regulated gene expression. J. Integ. Plant Biol. 49 1 (2007) 11-20
197. Litts J.C., Kelly J.M., and Lagarias J.C. Structure-function studies on phytochrome. J. Biol. Chem. 258 18 (1983) 11025-11031