Degradation of Arabidopsis CRY2 is regulated by SPA proteins and phytochrome A

Plant Cell

Volumn 24, Issue 6, 2012, Pages 2610-2623

  Weidler, Guido ^a   Oven Krockhaus, Sven Zur ^b   Heunemann, Michael ^b   Orth, Christian ^a   Schleifenbaum, Frank ^b   Harter, Klaus ^b   Hoecker, Ute ^c   Batschauer, Alfred ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864458848     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.098210     Document Type: Article

References (90)

1. 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.
2. Ahmad, M., Jarillo, J.A., and Cashmore, A.R. (1998). Chimeric proteins between cry1 and cry2 Arabidopsis blue light photo receptors indicate overlapping functions and varying protein stability. Plant Cell 10: 197-207.
3. Banerjee, R., Schleicher, E., Meier, S., Viana, R.M., Pokorny, R., Ahmad, M., Bittl, R., and Batschauer, A. (2007). The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J. Biol. Chem. 282: 14916-14922.
4. Batschauer, A. (1993). A plant gene for photolyase: An enzyme catalyzing the repair of UV-light-induced DNA damage. Plant J. 4: 705-709.
5. Bayram, O., Biesemann, C., Krappmann, S., Galland, P., and Braus, G.H. (2008). More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development. Mol. Biol. Cell 19: 3254-3262.
6. Bouly, J.P., Giovani, B., Djamei, A., Mueller, M., Zeugner, A., Dudkin, E.A., Batschauer, A., and Ahmad, M. (2003). Novel ATP-binding and autophosphorylation activity associated with Arabidopsis and human cryptochrome-1. Eur. J. Biochem. 270: 2921-2928.
7. Bouly, J.P., Schleicher, E., Dionisio-Sese, M., Vandenbussche, F., Van Der Straeten, D., Bakrim, N., Meier, S., Batschauer, A., Galland, P., Bittl, R., and Ahmad, M. (2007). Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol. Chem. 282: 9383-9391.
8. Brautigam, C.A., Smith, B.S., Ma, Z., Palnitkar, M., Tomchick, D.R., Machius, M., and Deisenhofer, J. (2004). Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101: 12142-12147.
9. Brudler, R., Hitomi, K., Daiyasu, H., Toh, H., Kucho, K., Ishiura, M., Kanehisa, M., Roberts, V.A., Todo, T., Tainer, J.A., and Getzoff, E.D. (2003). Identification of a new cryptochrome class. Structure, function, and evolution. Mol. Cell 11: 59-67.
10. Brunelle, S.A., Starr Hazard, E., Sotka, E.E., and Van Dolah, F.M. (2007). Characterization of a dinoflagellate Cryptochrome blue-light receptor with a possible role in a circadian control of the cell cycle. J. Phycol. 42: 509-518.
11. Cashmore, A.R. (2003). Cryptochromes: Enabling plants and animals to determine circadian time. Cell 114: 537-543.
12. 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.
13. 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.
14. Clough, R.C., Jordan-Beebe, E.T., Lohman, K.N., Marita, J.M., Walker, J.M., Gatz, C., and Vierstra, R.D. (1999). Sequences within both the N-and C-terminal domains of phytochrome A are required for PFR ubiquitination and degradation. Plant J. 17: 155-167.
15. Clough, R.C., and Viestra, R.D. (1997). Phytochrom degradation. Plant Cell Environ. 20: 713-721.
16. Dehesh, K., Franci, C., Parks, B.M., Seeley, K.A., Short, T.W., Tepperman, J.M., and Quail, P.H. (1993). Arabidopsis HY8 locus encodes phytochrome A. Plant Cell 5: 1081-1088.
17. Duek, P.D., Elmer, M.V., van Oosten, V.R., and Fankhauser, C. (2004). The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr. Biol. 14: 2296-2301.
18. El-Din El-Assal, S., Alonso-Blanco, C., Peeters, A.J., Raz, V., and Koornneef, M. (2001). A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat. Genet. 29: 435-440.
19. Exner, V., Alexandre, C.M., Rosenfeldt, G., Alfarano, P., Nater, M., Caflisch, A., Gruissem, W., Batschauer, A., and Hennig, L. (2010). A gain-of-function mutation of Arabidopsis cryptochrome1 promotes flowering. Plant Physiol. 154: 1633-1645.
20. Fittinghoff, K., Laubinger, S., Nixdorf, M., Fackendahl, P., Baumgardt, R.L., Batschauer, A., and Hoecker, U. (2006). Functional and expression analysis of Arabidopsis SPA genes during seedling photomorphogenesis and adult growth. Plant J. 47: 577-590.
21. Folta, K.M., Pontin, M.A., Karlin-Neumann, G., Bottini, R., and Spalding, E.P. (2003). Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. Plant J. 36: 203-214.
22. Froehlich, A.C., Chen, C.H., Belden, W.J., Madeti, C., Roenneberg, T., Merrow, M., Loros, J.J., and Dunlap, J.C. (2010). Genetic and molecular characterization of a cryptochrome from the filamentous fungus Neurospora crassa. Eukaryot. Cell 9: 738-750.
23. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M.R. (2010). A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64: 355-365.
24. Grefen, C., Städele, K., Růzicka, K., Obrdlik, P., Harter, K., and Horák, J. (2008). Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol. Plant 1: 308-320.
25. Guo, H., Duong, H., Ma, N., and Lin, C. (1999). The Arabidopsis blue light receptor cryptochrome 2 is a nuclear protein regulated by a blue light-dependent post-transcriptional mechanism. Plant J. 19: 279-287.
26. Guo, H., Yang, H., Mockler, T.C., and Lin, C. (1998). Regulation of flowering time by Arabidopsis photoreceptors. Science 279: 1360-1363.
27. Harter, K., Meixner, A.J., and Schleifenbaum, F. (2012). Spectro microscopy of living plant cells. Mol. Plant 5: 14-26.
28. Hayama, R., and Coupland, G. (2004). The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol. 135: 677-684.
29. Heijde, M. et al. (2010). Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant Cell Environ. 33: 1614-1626.
30. Hoang, N., Bouly, J.P., and Ahmad, M. (2008). Evidence of a lightsensing role for folate in Arabidopsis cryptochrome blue-light receptors. Mol. Plant 1: 68-74.
31. Hoecker, U. (2005). Regulated proteolysis in light signaling. Curr. Opin. Plant Biol. 8: 469-476.
32. Hoecker, U., and Quail, P.H. (2001). The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis. J. Biol. Chem. 276: 38173-38178.
33. Hoecker, U., Tepperman, J.M., and Quail, P.H. (1999). SPA1, a WDrepeat protein specific to phytochrome A signal transduction. Science 284: 496-499.
34. Hoecker, U., Xu, Y., and Quail, P.H. (1998). SPA1: A new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell 10: 19-33.
35. Jang, I.C., Henriques, R., Seo, H.S., Nagatani, A., and Chua, N.H. (2010). Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22: 2370-2383.
36. Jang, I.C., Yang, J.Y., Seo, H.S., and Chua, N.H. (2005). HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 19: 593-602.
37. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
38. Kennedy, M.J., Hughes, R.M., Peteya, L.A., Schwartz, J.W., Ehlers, M.D., and Tucker, C.L. (2010). Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 7: 973-975.
39. Kleine, T., Lockhart, P., and Batschauer, A. (2003). An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J. 35: 93-103.
40. Kleiner, O., Kircher, S., Harter, K., and Batschauer, A. (1999). Nuclear localization of the Arabidopsis blue light receptor cryptochrome 2. Plant J. 19: 289-296.
41. Lariguet, P., and Fankhauser, C. (2004). Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J. 40: 826-834.
42. Laubinger, S., Fittinghoff, K., and Hoecker, U. (2004). The SPA quartet: A family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell 16: 2293-2306.
43. Laubinger, S., and Hoecker, U. (2003). The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light. Plant J. 35: 373-385.
44. Laubinger, S., Marchal, V., Le Gourrierec, J., Wenkel, S., Adrian, J., Jang, S., Kulajta, C., Braun, H., Coupland, G., and Hoecker, U. (2006). Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133: 3213-3222. Erratum. Development 133: 4608.
45. Leivar, P., Monte, E., Al-Sady, B., Carle, C., Storer, A., Alonso, J.M., Ecker, J.R., and Quail, P.H. (2008). The Arabidopsis phyto chrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20: 337-352.
46. Lian, H.L., He, S.B., Zhang, Y.C., Zhu, D.M., Zhang, J.Y., Jia, K.P., Sun, 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.
47. Lin, C., Yang, H., Guo, H., Mockler, T., Chen, J., and Cashmore, A.R. (1998). Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc. Natl. Acad. Sci. USA 95: 2686-2690.
48. Liu, B., Liu, H., Zhong, D., and Lin, C. (2010). Searching for a photocycle of the cryptochrome photoreceptors. Curr. Opin. Plant Biol. 13: 578-586.
49. 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.
50. 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.
51. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
52. Ma, L., Li, J., Qu, L., Hager, J., Chen, Z., Zhao, H., and Deng, X.W. (2001). Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13: 2589-2607.
53. Malhotra, K., Kim, S.T., Batschauer, A., Dawut, L., and Sancar, A. (1995). Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis alba with a high degree of sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity. Biochemistry 34: 6892-6899.
54. McNellis, T.W., von Arnim, A.G., Araki, T., Komeda, Y., Miséra, S., and Deng, X.W. (1994). Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6: 487-500.
55. Mockler, T., Yang, H., Yu, X., Parikh, D., Cheng, Y.C., Dolan, S., and Lin, C. (2003). Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc. Natl. Acad. Sci. USA 100: 2140-2145.
56. Moldt, J., Pokorny, R., Orth, C., Linne, U., Geisselbrecht, Y., Marahiel, M.A., Essen, L.O., and Batschauer, A. (2009). Photoreduction of the folate cofactor in members of the photolyase family. J. Biol. Chem. 284: 21670-21683.
57. Müller, M., and Carell, T. (2009). Structural biology of DNA photolyases and cryptochromes. Curr. Opin. Struct. Biol. 19: 277-285.
58. Ohgishi, M., Saji, K., Okada, K., and Sakai, T. (2004). Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc. Natl. Acad. Sci. USA 101: 2223-2228.
59. Osterlund, M.T., Wei, N., and Deng, X.W. (2000). The roles of photoreceptor systems and the COP1-targeted destabilization of HY5 in light control of Arabidopsis seedling development. Plant Physiol. 124: 1520-1524.
60. Phee, B.K., Park, S., Cho, J.H., Jeon, J.S., Bhoo, S.H., and Hahn, T.R. (2007). Comparative proteomic analysis of blue light signaling components in the Arabidopsis cryptochrome 1 mutant. Mol. Cells 23: 154-160.
61. Pokorny, R., Klar, T., Hennecke, U., Carell, T., Batschauer, A., and Essen, L.O. (2008). Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc. Natl. Acad. Sci. USA 105: 21023-21027.
62. Reed, J.W., Nagatani, A., Elich, T.D., Fagan, M., and Chory, J. (1994). Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol. 104: 1139-1149.
63. Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M., and Chory, J. (1993). Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5: 147-157.
64. Saijo, Y., Sullivan, J.A., Wang, H., Yang, J., Shen, Y., Rubio, V., Ma, L., Hoecker, U., and Deng, X.W. (2003). The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev. 17: 2642-2647.
65. Sancar, A. (2003). Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103: 2203-2237.
66. Schütze, K., Harter, K., and Chaban, C. (2009). Bimolecular fluorescence complementation (BiFC) to study protein-protein interactions in living plant cells. Methods Mol. Biol. 479: 189-202.
67. Searle, I., and Coupland, G. (2004). Induction of flowering by seasonal changes in photoperiod. EMBO J. 23: 1217-1222.
68. Selby, C.P., and Sancar, A. (2006). A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc. Natl. Acad. Sci. USA 103: 17696-17700.
69. Seo, H.S., Yang, J.Y., Ishikawa, M., Bolle, C., Ballesteros, M.L., and Chua, N.H. (2003). LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423: 995-999.
70. 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.
71. 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.
72. Sharrock, R.A., and Clack, T. (2002). Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 130: 442-456.
73. Shinomura, T., Nagatani, A., Hanzawa, H., Kubota, M., Watanabe, M., and Furuya, M. (1996). Action spectra for phytochrome A and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93: 8129-8133.
74. Somers, D.E., Devlin, P.F., and Kay, S.A. (1998). Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282: 1488-1490.
75. Subramanian, C., Xu, Y., Johnson, C.H., and von Arnim, A.G. (2004). In vivo detection of protein-protein interaction in plant cells using BRET. Methods Mol. Biol. 284: 271-286.
76. Tóth, R., Kevei, E., Hall, A., Millar, A.J., Nagy, F., and Kozma-Bognár, L. (2001). Circadian clock-regulated expression of phyto-chrome and cryptochrome genes in Arabidopsis. Plant Physiol. 127: 1607-1616.
77. Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coupland, G. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003-1006.
78. Voinnet, O., Lederer, C., and Baulcombe, D.C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157-167.
79. Wang, H., Ma, L.G., Li, J.M., Zhao, H.Y., and Deng, X.W. (2001). Direct interaction of Arabidopsis cryptochromes with COP1 in light control development. Science 294: 154-158.
80. Wanke, D., Hohenstatt, M.L., Dynowski, M., Bloss, U., Hecker, A., Elgass, K., Hummel, S., Hahn, A., Caesar, K., Schleifenbaum, F., Harter, K., and Berendzen, K.W. (2011). Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus. PLoS ONE 6: e16070.
81. 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.
82. 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.
83. Yang, H.Q., Wu, Y.J., Tang, R.H., Liu, D., Liu, Y., and Cashmore, A.R. (2000). The C termini of Arabidopsis cryptochromes mediate a constitutive light response. Cell 103: 815-827.
84. Yang, J., Lin, R., Sullivan, J., Hoecker, U., Liu, B., Xu, L., Deng, X.W., and Wang, H. (2005). Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell17: 804-821.
85. Yanovsky, M.J., and Kay, S.A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308-312.
86. Yanovsky, M.J., Mazzella, M.A., and Casal, J.J. (2000). A quadruple photoreceptor mutant still keeps track of time. Curr. Biol. 10: 1013-1015.
87. Yu, X., Klejnot, J., Zhao, X., Shalitin, D., Maymon, M., Yang, H., Lee, J., Liu, X., Lopez, J., and Lin, C. (2007). Arabidopsis crypto-chrome 2 completes its posttranslational life cycle in the nucleus. Plant Cell 19: 3146-3156.
88. Yu, X., Sayegh, R., Maymon, M., Warpeha, K., Klejnot, J., Yang, H., Huang, J., Lee, J., Kaufman, L., and Lin, C. (2009). Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation. Plant Cell 21: 118-130.
89. Zhu, D., Maier, A., Lee, J.H., Laubinger, S., Saijo, Y., Wang, H., Qu, L.J., Hoecker, U., and Deng, X.W. (2008). Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 20: 2307-2323.
90. 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.