Phytochrome signaling mechanisms and the control of plant development

Trends in Cell Biology

Volumn 21, Issue 11, 2011, Pages 664-671

  Chen, Meng ^a   Chory, Joanne ^b,c  

^a DUKE UNIVERSITY   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOCHROME A; PHYTOCHROME B; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE E3;

ARABIDOPSIS; CELL NUCLEUS; CYTOPLASM; LIGHT; NONHUMAN; PHOTOMORPHOGENESIS; PLANT DEVELOPMENT; PRIORITY JOURNAL; REVIEW;

CELL NUCLEUS; CULLIN PROTEINS; DOWN-REGULATION; LIGHT; MORPHOGENESIS; PHYTOCHROME A; PHYTOCHROME B; PLANT PROTEINS; PLANTS; PROTEIN TRANSPORT; SEEDLING; SIGNAL TRANSDUCTION;

EID: 80755129056     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2011.07.002     Document Type: Review

References (117)

1. Chen M., et al. Light signal transduction in higher plants. Annu. Rev. Genet. 2004, 38:87-117.
2. Jiao Y., et al. Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 2007, 8:217-230.
3. Hu W., et al. A light-independent allele of phytochrome B faithfully recapitulates photomorphogenic transcriptional networks. Mol. Plant 2009, 2:166-182.
4. Tepperman J.M., et al. phyA dominates in transduction of red-light signals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation. Plant J. 2006, 48:728-742.
5. Leivar P., et al. Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 2009, 21:3535-3553.
6. Shin J., et al. Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:7660-7665.
7. Nagatani A. Phytochrome: structural basis for its functions. Curr. Opin. Plant Biol. 2010, 13:565-570.
8. Rockwell N.C., et al. Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 2006, 57:837-858.
9. Ulijasz A.T., et al. Structural basis for the photoconversion of a phytochrome to the activated Pfr form. Nature 2010, 463:250-254.
10. Fankhauser C., Chen M. Transposing phytochrome into the nucleus. Trends Plant Sci. 2008, 13:596-601.
11. Clack T., et al. Obligate heterodimerization of Arabidopsis phytochromes C and E and interaction with the PIF3 basic helix-loop-helix transcription factor. Plant Cell 2009, 21:786-799.
12. Kami C., et al. Light-regulated plant growth and development. Curr. Top. Dev. Biol. 2010, 91:29-66.
13. Franklin K.A., Quail P.H. Phytochrome functions in Arabidopsis development. J. Exp. Bot. 2010, 61:11-24.
14. Clough R., Vierstra R. Phytochrome degradation. Plant Cell Environ. 1997, 20:713-721.
15. Chory J. Light signal transduction: an infinite spectrum of possibilities. Plant J. 2010, 61:982-991.
16. Chory J., et al. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 1989, 58:991-999.
17. Deng X.W., et al. cop1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 1991, 5:1172-1182.
18. Serino G., Deng X.W. The COP9 signalosome: regulating plant development through the control of proteolysis. Annu. Rev. Plant Biol. 2003, 54:165-182.
19. Laubinger S., et al. The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell 2004, 16:2293-2306.
20. Leivar P., et al. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr. Biol. 2008, 18:1815-1823.
21. Su Y.S., Lagarias J.C. Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 2007, 19:2124-2139.
22. Whitelam G.C., et al. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 1993, 5:757-768.
23. Desnos T., et al. FHY1: a phytochrome A-specific signal transducer. Genes Dev. 2001, 15:2980-2990.
24. Wang H., Deng X.W. Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. EMBO J. 2002, 21:1339-1349.
25. Ballesteros M.L., et al. LAF1, a MYB transcription activator for phytochrome A signaling. Genes Dev. 2001, 15:2613-2625.
26. Hudson M., et al. The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev. 1999, 13:2017-2027.
27. Fairchild C.D., et al. HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev. 2000, 14:2377-2391.
28. Koornneef M., et al. Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z. Pflanzenphysiol. 1980, 100:147-160.
29. Oyama T., et al. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 1997, 11:2983-2995.
30. Chen M., et al. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 2010, 141:1230-1240.
31. Strasser B., et al. Arabidopsis thaliana life without phytochromes. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4776-4781.
32. Sakamoto K., Nagatani A. Nuclear localization activity of phytochrome B. Plant J. 1996, 10:859-868.
33. Yamaguchi R., et al. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J. Cell Biol. 1999, 145:437-445.
34. Kircher S., et al. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 1999, 11:1445-1456.
35. Kircher S., et al. 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.
36. Kim L., et al. Light-induced nuclear import of phytochrome-A:GFP fusion proteins is differentially regulated in transgenic tobacco and Arabidopsis. Plant J. 2000, 22:125-133.
37. Bauer D., et al. Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 2004, 16:1433-1445.
38. Chen M., et al. Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Curr. Biol. 2005, 15:637-642.
39. Hiltbrunner A., et al. Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr. Biol. 2005, 15:2125-2130.
40. Hiltbrunner A., et al. FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant Cell Physiol. 2006, 47:1023-1034.
41. Genoud T., et al. FHY1 mediates nuclear import of the light-activated phytochrome A photoreceptor. PLoS Genet. 2008, 4:e1000143.
42. Saijo Y., et al. Arabidopsis COP1/SPA1 complex and FHY1/FHY3 associate with distinct phosphorylated forms of phytochrome A in balancing light signaling. Mol. Cell 2008, 31:607-613.
43. 1 to transmit phytochrome A signals for inhibition of hypocotyl elongation. Plant Cell 2009, 21:1341-1359.
44. 1 protein stability is regulated by light via phytochrome A and 26S proteasome. Plant Physiol. 2005, 139:1234-1243.
45. Shen Y., et al. Phytochrome A mediates rapid red light-induced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in a low fluence response. Plant Cell 2009, 21:494-506.
46. Lin R., et al. Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 2007, 318:1302-1305.
47. Lin R., et al. Discrete and essential roles of the multiple domains of Arabidopsis FHY3 in mediating phytochrome A signal transduction. Plant Physiol. 2008, 148:981-992.
48. Li J., et al. Arabidopsis transcription factor ELONGATED HYPOCOTYL5 plays a role in the feedback regulation of phytochrome a signaling. Plant Cell 2010, 22:3634-3649.
49. Chen M. Phytochrome nuclear body: an emerging model to study interphase nuclear dynamics and signaling. Curr. Opin. Plant Biol. 2008, 11:503-508.
50. Al-Sady B., et al. Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 2006, 23:439-446.
51. Leivar P., et al. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 2008, 20:337-352.
52. Oka Y., et al. Mutant screen distinguishes between residues necessary for light-signal perception and signal transfer by phytochrome B. PLoS Genet. 2008, 4:e1000158.
53. Kikis E.A., et al. Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3. PLoS Genet. 2009, 5:e1000352.
54. Chen M., et al. Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14493-14498.
55. Rausenberger J., et al. An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS ONE 2010, 5:e10721.
56. Matsushita T., et al. Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 2003, 424:571-574.
57. Palagyi A., et al. Functional analysis of amino-terminal domains of the photoreceptor phytochrome B. Plant Physiol. 2010, 153:1834-1845.
58. 1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 2005, 19:593-602.
59. Ang L.H., et al. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1998, 1:213-222.
60. Seo H.S., et al. LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 2003, 423:995-999.
61. Seo H.S., et al. Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev. 2004, 18:617-622.
62. Sharrock R.A., Clack T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 2002, 130:442-456.
63. Canton F.R., Quail P.H. Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis. Plant Physiol. 1999, 121:1207-1216.
64. Jang I.C., et al. Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus. Plant Cell 2011, 23:459-470.
65. Jang I.C., et al. Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 2010, 22:2370-2383.
66. Quail P.H. The phytochromes: a biochemical mechanism of signaling in sight?. Bioessays 1997, 19:571-579.
67. Chen H., et al. Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 2010, 22:108-123.
68. Zhu D., et al. Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 2008, 20:2307-2323.
69. Quint M., et al. Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J. 2005, 43:371-383.
70. Rosler J., et al. Arabidopsis fhl/fhy1 double mutant reveals a distinct cytoplasmic action of phytochrome A. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10737-10742.
71. Toledo-Ortiz G., et al. Subcellular sites of the signal transduction and degradation of phytochrome A. Plant Cell Physiol. 2010, 51:1648-1660.
72. Debrieux D., Fankhauser C. Light-induced degradation of phyA is promoted by transfer of the photoreceptor into the nucleus. Plant Mol. Biol. 2010, 73:687-695.
73. Wolf I., et al. Light-regulated nuclear import and degradation of Arabidopsis phytochrome-A N-terminal fragments. Plant Cell Physiol. 2011, 52:361-372.
74. Clack T., et al. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol. Biol. 1994, 25:413-427.
75. Al-Sady B., et al. Mechanistic duality of transcription factor function in phytochrome signaling. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2232-2237.
76. Leivar P., Quail P.H. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 2011, 16:19-28.
77. Pepper A., et al. DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 1994, 78:109-116.
78. Deng X.W., et al. COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 1992, 71:791-801.
79. Suzuki G., et al. Arabidopsis COP10 is a ubiquitin-conjugating enzyme variant that acts together with COP1 and the COP9 signalosome in repressing photomorphogenesis. Genes Dev. 2002, 16:554-559.
80. Hoecker U., et al. SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 1999, 284:496-499.
81. Schroeder D.F., et al. De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 2002, 12:1462-1472.
82. Chen H., et al. Arabidopsis CULLIN4 Forms an E3 Ubiquitin Ligase with RBX1 and the CDD Complex in Mediating Light Control of Development. Plant Cell 2006, 18:1991-2004.
83. Biedermann S., Hellmann H. WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci. 2011, 16:38-46.
84. Lee J.H., et al. Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 2008, 20:152-167.
85. Osterlund M.T., et al. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 2000, 405:462-466.
86. Duek P.D., et al. The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr. Biol. 2004, 14:2296-2301.
87. Yang J., et al. Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 2005, 17:804-821.
88. 105, activates a branch pathway of light signaling in Arabidopsis. Plant Physiol. 2003, 133:1630-1642.
89. 5 activity. Genes Dev. 2003, 17:2642-2647.
90. Nixdorf M., Hoecker U. SPA1 and DET1 act together to control photomorphogenesis throughout plant development. Planta 2010, 231:825-833.
91. von Arnim A.G., Deng X.W. Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 1994, 79:1035-1045.
92. Chamovitz D.A., et al. The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 1996, 86:115-121.
93. von Arnim A.G., et al. Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol. 1997, 114:779-788.
94. Wang X., et al. Regulation of COP1 nuclear localization by the COP9 signalosome via direct interaction with CSN1. Plant J. 2009, 58:655-667.
95. Balcerowicz M., et al. Light exposure of Arabidopsis seedlings causes rapid de-stabilization as well as selective post-translational inactivation of the repressor of photomorphogenesis SPA2. Plant J. 2011, 65:712-723.
96. Zuo Z., et al. Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral Initiation in Arabidopsis. Curr. Biol. 2011, 21:841-847.
97. Liu B., et al. Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev. 2011, 25:1029-1034.
98. Lian H.L., et al. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev. 2011, 25:1023-1028.
99. Ni M., et al. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 1998, 95:657-667.
100. Huq E., Quail P.H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002, 21:2441-2450.
101. Huq E., et al. Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 2004, 305:1937-1941.
102. Hornitschek P., et al. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 2009, 28:3893-3902.
103. Moon J., et al. PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9433-9438.
104. de Lucas M., et al. A molecular framework for light and gibberellin control of cell elongation. Nature 2008, 451:480-484.
105. Oh E., et al. Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 2009, 21:403-419.
106. Oh E., et al. PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 2004, 16:3045-3058.
107. Fujimori T., et al. Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 2004, 45:1078-1086.
108. Khanna R., et al. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 2004, 16:3033-3044.
109. Lorrain S., et al. Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 2009, 60:449-461.
110. Stephenson P.G., et al. PIF3 is a repressor of chloroplast development. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:7654-7659.
111. Toledo-Ortiz G., et al. Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11626-11631.
112. Bu Q., et al. Phosphorylation by CK2 enhances the rapid light-induced degradation of phytochrome interacting factor 1 in Arabidopsis. J. Biol. Chem. 2011, 286:12066-12074.
113. Shen H., et al. Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 2008, 20:1586-1602.
114. Lorrain S., et al. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2008, 53:312-323.
115. Nozue K., et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 2007, 448:358-361.
116. Shen Y., et al. Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 2007, 145:1043-1051.
117. Shen H., et al. PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 2005, 44:1023-1035.