Lifetimes of Arabidopsis cryptochrome signaling states in vivo

Plant Journal

Volumn 74, Issue 4, 2013, Pages 583-592

  Herbel, Vera ^a   Orth, Christian ^a   Wenzel, Ringo ^b,e   Ahmad, Margaret ^c,d   Bittl, Robert ^b   Batschauer, Alfred ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c SORBONNE UNIVERSITÉ   (France)

^d XAVIER UNIVERSITY   (United States)

^e CARL ZEISS SMT AG   (Germany)

Author keywords

Arabidopsis thaliana; cryptochrome; electron paramagnetic resonance; flavin radical; photoreceptor lifetime; signaling state

Indexed keywords

ARABIDOPSIS THALIANA; CRYPTOCHROMES; FLAVIN RADICAL; PHOTORECEPTOR LIFETIME; SIGNALING STATE;

CHROMOPHORES; ELECTRON RESONANCE; PARAMAGNETIC RESONANCE; PARAMAGNETISM; SIGNALING; VISION;

CELL SIGNALING;

ARABIDOPSIS PROTEIN; CRY1 PROTEIN, ARABIDOPSIS; CRY2 PROTEIN, ARABIDOPSIS; CRYPTOCHROME; DRUG DERIVATIVE; FLAVIN SEMIQUINONE; FLAVINE ADENINE NUCLEOTIDE; VISUAL PROTEINS AND PIGMENTS;

ANIMAL; ARABIDOPSIS; ARTICLE; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; INSECT; LIGHT; METABOLISM; MUTATION; PHOTOTRANSDUCTION; PHYSIOLOGY; RADIATION EXPOSURE; REPORTER GENE; SEEDLING; TIME; TRANSGENIC PLANT;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL LINE; CRYPTOCHROMES; FLAVIN-ADENINE DINUCLEOTIDE; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; INSECTS; LIGHT; LIGHT SIGNAL TRANSDUCTION; MUTATION; PHOTORECEPTORS, PLANT; PLANTS, GENETICALLY MODIFIED; SEEDLING; TIME FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HEXAPODA;

EID: 84877719536     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12144     Document Type: Article

References (71)

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., and, Cashmore, A.R., (1997) The blue-light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thaliana. Plant J. 11, 421-427.
3. Ahmad, M., Lin, C., and, Cashmore, A.R., (1995) Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J. 8, 653-658.
4. Ahmad, M., Jarillo, J.A., and, Cashmore, A.R., (1998) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell, 10, 197-207.
5. Ahmad, M., Grancher, N., Heil, M., Black, R.C., Giovani, B., Galland, P., and, Lardemer, D., (2002) Action spectrum for cryptochrome-dependent hypocotyl growth inhibition in Arabidopsis. Plant Physiol. 129, 774-785.
6. 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.
7. Batschauer, A., Rocholl, M., Kaiser, T., Nagatani, A., Furuya, M., and, Schäfer, E., (1996) Blue and UV-A light regulated CHS expression in Arabidopsis independent of phytochrome A and phytochrome B. Plant J. 9, 63-69.
8. 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.
9. Bouly, J.P., Schleicher, E., Dionisio-Sese, M., et al. (2007) Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol. Chem. 282, 9383-9391.
10. Briggs, W.R., and, Christie, J.M., (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 7, 204-210.
11. Brudler, R., Hitomi, K., Daiyasu, H., et al. (2003) Identification of a new cryptochrome class. Structure, function, and evolution. Mol. Cell 11, 59-67.
12. Burney, S., Hoang, N., Caruso, M., Dudkin, E.A., Ahmad, M., and, Bouly, J.P., (2009) Conformational change induced by ATP binding correlates with enhanced biological function of Arabidopsis cryptochrome. FEBS Lett. 583, 1427-1433.
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. Christie, J.M., and, Jenkins, G.I., (1996) Distinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells. Plant Cell, 8, 1555-1567.
15. Christie, J.M., Arvai, A.S., Baxter, K.J., et al. (2012) Plant UVR8 photoreceptors senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science, 335, 1492-1496.
16. Demarsy, E., and, Fankhauser, C., (2009) Higher plants use LOV to perceive blue light. Curr. Opin. Plant Biol. 12, 69-74.
17. Eichenberg, K., Kunkel, T., Kretsch, T., Speth, V., and, Schäfer, E., (1999) In vivo characterization of chimeric phytochromes in yeast. J. Biol. Chem. 274, 354-359.
18. Eichenberg, K., Bäuerle, I., Paulo, N., Sharrock, R.A., Rüdiger, W., and, Schäfer, E., (2000) Arabidopsis phytochromes C and E have different spectral characteristics from those of phytochromes A and B. FEBS Lett. 470, 107-112.
19. El-Assal, S. E-D., 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.
20. Feinbaum, R.L., and, Ausubel, F.M., (1988) Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol. Cell. Biol. 8, 1985-1992.
21. Feinbaum, R.L., Storz, G., and, Ausubel, F.M., (1991) High intensity and blue light regulated expression of chimeric chalcone synthase genes in transgenic Arabidopsis thaliana plants. Mol. Gen. Genet. 226, 449-456.
22. Fuglevand, G., Jackson, J.A., and, Jenkins, G.I., (1996) UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell, 8, 2347-2357.
23. Guo, H., Yang, H., Mockler, T.C., and, Lin, C., (1998) Regulation of flowering time by Arabidopsis photoreceptors. Science, 279, 1360-1363.
24. Hartmann, U., Valentine, W.J., Christie, J.M., Hays, J., Jenkins, G.I., and, Weisshaar, B., (1998) Identification of UV/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system. Plant Mol. Biol. 36, 741-754.
25. Hennig, L., Büche, C., Eichenberg, K., and, Schäfer, E., (1999) Dynamic properties of endogenous phytochrome A in Arabidopsis seedlings. Plant Physiol. 121, 571-577.
26. Hennig, L., Büche, C., and, Schäfer, E., (2000) Degradation of phytochrome A and the high irradiance response in Arabidopsis: a kinetic analysis. Plant, Cell Environ. 23, 727-734.
27. Hoang, N., Schleicher, E., Kacprzak, S., Bouly, J.P., Picot, M., Wu, W., Berndt, A., Wolf, E., Bittl, R., and, Ahmad, M., (2008) Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol. 6, e160.
28. Immeln, D., Schlesinger, R., Heberle, J., and, Kottke, T., (2007) Blue light induces radical formation and autophosphorylation in the light-sensitive domain of Chlamydomonas cryptochrome. J. Biol. Chem. 282, 21720-21728.
29. Jackson, J.A., and, Jenkins, G.I., (1995) Extension-growth responses and expression of flavonoid biosynthesis genes in the Arabidopsis hy4 mutant. Planta, 197, 233-239.
30. Jefferson, R.A., (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387-405.
31. Kaiser, T., and, Batschauer, A., (1995) Cis-acting elements of the CHS1 gene from white mustard controlling promoter activity and spatial patterns of expression. Plant Mol. Biol. 28, 231-243.
32. 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.
33. 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.
34. Koh, K., Zheng, X., and, Sehgal, A., (2006) JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science, 312, 1809-1812.
35. Kondoh, M., Shiraishi, C., Müller, P., Ahmad, M., Hitomi, K., Getzoff, E.D., and, Terazima, M., (2011) Light-induced conformational changes in full-length Arabidopsis thaliana cryptochrome. J. Mol. Biol. 413, 128-137.
36. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
37. Lange, H., Shropshire, W. Jr, and, Mohr, H., (1971) An analysis of phytochrome-mediated anthocyanin synthesis. Plant Physiol. 47, 649-655.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Mancinelli, A.L., (1994) The physiology of phytochrome action. In Photomorphogenesis in Plants (, Kendrick, R.E., and, Kronenberg, G.H.M., eds). Dodrecht: Kluwer Academic Publishers, pp. 211-269.
44. Martin, C.R., (1993) Structure, function, and regulation of the chalcone synthase. Int. Rev. Cytol. 147, 233-284.
45. Mathur, J., and, Koncz, C.S., (1998) Establishment and maintenance of cell suspension cultures. In Methods in Molecular Biology, Vol. 82 Arabidopsis Protocols (, Martinez-Zapater, J., and, Salinas, J., eds). Totowa: Humana Press, pp. 27-30.
46. Müller, 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.
47. Ohl, S., Hahlbrock, K., and, Schäfer, E., (1989) A stable blue-light-derived signal modulates ultraviolet-light induced activation of the chalcone synthase gene in cultured parsley cells. Planta, 177, 228-236.
48. Ozturk, N., Selby, C.P., Annayev, Y., Zhong, D., and, Sancar, A., (2011) Reaction mechanism of Drosophila cryptochrome. Proc. Natl Acad. Sci. USA 108, 516-521.
49. Partch, C.L., Clarkson, M.W., Özgür, S., Lee, A.L., and, Sancar, A., (2005) Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor. Biochemistry, 44, 3795-3805.
50. 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.
51. Rizzini, L., Favory, J.-J., Cloix, C., et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science, 332, 103-106.
52. Rockwell, N.C., Su, J.-S., and, Lagarias, J.C., (2006) Phytochrome structure and signaling mechanism. Annu. Rev. Plant Biol. 57, 837-858.
53. Rosenfeldt, G., Muñoz Viana, R., von Arnim, A.G., Mootz, H.D., and, Batschauer, A., (2008) Chemically induced and light-independent cryptochrome photoreceptor activation. Mol. Plant 1, 4-14.
54. Sancar, A., (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103, 2203-2237.
55. Sang, Y., Li, Q.H., Rubio, V., Zhang, Y.C., Mao, J., Deng, X.-W., and, Yang, H.Q., (2005) N-terminal domain-mediated homodimerization is required for photoreceptor activity of cryptochrome 1. Plant Cell, 17, 1569-1584.
56. Schaffner, W., and, Weissmann, C., (1973) A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 65, 502-514.
57. 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.
58. Sellaro, R., Crepy, M., Trupkin, S.A., Karayekov, E., Buchovsky, A.S., Ross, C., and, Casal, J.J., (2010) Cryptochrome as a sensor of blue/green ratio of natural radiation in Arabidopsis. Plant Physiol. 154, 401-409.
59. 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.
60. 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.
61. Sweere, U., Eichenberg, K., Lohrmann, J., Mira-Rodado, V., Bäuerle, I., Kudla, J., Nagy, F., Schäfer, E., and, Harter, K., (2001) Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science, 294, 1108-1111.
62. Vierstra, R.D., and, Quail, P.H., (1985) Spectral characterization and proteolytic mapping of native 120-kilodalton phytochrome from Cucurbita pepo L. Plant Physiol. 77, 990-998.
63. 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.
64. 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 mediated by SPA proteins and phytochrome A. Plant Cell, 24, 2610-2623.
65. Wu, D., Hu, Q., Yan, Z., et al. (2012) Structural basis of ultraviolet-B perception by UVR8. Nature, 484, 214-219.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. Zuo, Z., Meng, Y., Yu, X., Zhang, Z., Feng, D., Sun, S., Liu, B., and, Lin, C., (2012) A study of the blue-light-dependent phosphorylation, degradation, and photobody formation of Arabidopsis CRY2. Mol. Plant 5, 726-733.