Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis

Plant Cell

Volumn 25, Issue 2, 2013, Pages 535-544

  Medzihradszky, Mátyás ^a   Bindics, János ^a,b   Ádám, Éva ^b   Viczián, András ^b   Klement, Éva ^b   Lorrain, Séverine ^c   Gyula, Péter ^d   Mérai, Zsuzsanna ^a   Fankhauser, Christian ^c   Medzihradszky, Katalin F ^b   Kunkel, Tim ^a   Schäfer, Eberhard ^a   Nagy, Ferenc ^b,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84875525891     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.106898     Document Type: Article

References (50)

1. Ádám, É., Hussong, A., Bindics, J., Wüst, F., Viczián, A., Essing, M., Medzihradszky, M., Kircher, S., Schäfer, E., and Nagy, F. (2011). Altered dark-and photoconversion of phytochrome B mediate extreme light sensitivity and loss of photoreversibility of the phyB-401 mutant. PLoS ONE 6: e27250.
2. Ahmad, M., Jarillo, J.A., Smirnova, O., and Cashmore, A.R. (1998). The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol. Cell 1: 939-948.
3. Al-Sady, B., Ni, W.M., Kircher, S., Schäfer, E., and Quail, P.H. (2006). Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell 23: 439-446.
4. Bae, G., and Choi, G. (2008). Decoding of light signals by plant phytochromes and their interacting proteins. Annu. Rev. Plant Biol. 59: 281-311.
5. Bauer, D., Viczián, A., Kircher, S., Nobis, T., Nitschke, R., Kunkel, T., Panigrahi, K.C.S., Adám, É., Fejes, E., Schäfer, E., and Nagy, F. (2004). Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16: 1433-1445.
6. Chen, F., Shi, X., Chen, L., Dai, M., Zhou, Z., Shen, Y., Li, J., Li, G., Wei, N., and Deng, X.W. (2012). Phosphorylation of FAR-RED ELONGATED HYPOCOTYL1 is a key mechanism defining signaling dynamics of phytochrome A under red and far-red light in Arabidopsis. Plant Cell 24: 1907-1920.
7. Chen, M., Chory, J., and Fankhauser, C. (2004). Light signal transduction in higher plants. Annu. Rev. Genet. 38: 87-117.
8. Chen, M., Schwab, R., and Chory, J. (2003). Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc. Natl. Acad. Sci. USA 100: 14493-14498.
9. Cherry, J.R., Hondred, D., Walker, J.M., and Vierstra, R.D. (1992). Phytochrome requires the 6-kDa N-terminal domain for full biological activity. Proc. Natl. Acad. Sci. USA 89: 5039-5043.
10. Choi, G., Yi, H., Lee, J., Kwon, Y.K., Soh, M.S., Shin, B., Luka, Z., Hahn, T.R., and Song, P.S. (1999). Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401: 610-613.
11. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
12. Colón-Carmona, A., Chen, D.L., Yeh, K.C., and Abel, S. (2000). Aux/ IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol. 124: 1728-1738.
13. 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.
14. Elich, T.D., and Chory, J. (1997). Biochemical characterization of Arabidopsis wild-type and mutant phytochrome B holoproteins. Plant Cell 9: 2271-2280.
15. Fankhauser, C., Yeh, K.C., Lagarias, J.C., Zhang, H., Elich, T.D., and Chory, J. (1999). PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284: 1539-1541.
16. Han, Y.J., Kim, H.S., Kim, Y.M., Shin, A.Y., Lee, S.S., Bhoo, S.H., Song, P.S., and Kim, J.I. (2010). Functional characterization of phytochrome autophosphorylation in plant light signaling. Plant Cell Physiol. 51: 596-609.
17. Hiltbrunner, A., Viczián, A., Bury, E., Tscheuschler, A., Kircher, S., Tóth, R., Honsberger, A., Nagy, F., Fankhauser, C., and Schäfer, E. (2005). Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr. Biol. 15: 2125-2130.
18. Jordan, E.T., Marita, J.M., Clough, R.C., and Vierstra, R.D. (1997). Characterization of regions within the N-terminal 6-kilodalton domain of phytochrome A that modulate its biological activity. Plant Physiol. 115: 693-704.
19. Kikis, E.A., Oka, Y., Hudson, M.E., Nagatani, A., and Quail, P.H. (2009). Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3. PLoS Genet. 5: e1000352.
20. Kim, J.I., Shen, Y., Han, Y.J., Park, J.E., Kirchenbauer, D., Soh, M.S., Nagy, F., Schäfer, E., and Song, P.S. (2004). Phytochrome phosphorylation modulates light signaling by influencing the protein-protein interaction. Plant Cell 16: 2629-2640.
21. Kinoshita, E., and Kinoshita-Kikuta, E. (2011). Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics 11: 319-323.
22. Kircher, S., Kozma-Bognar, L., Kim, L., Ádám, E., Harter, K., Schäfer, E., and Nagy, F. (1999). Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11: 1445-1456.
23. Kretsch, T., Poppe, C., and Schäfer, E. (2000). A new type of mutation in the plant photoreceptor phytochrome B causes loss of photoreversibility and an extremely enhanced light sensitivity. Plant J. 22: 177-186.
24. Kunkel, T., Speth, V., Büche, C., and Schäfer, E. (1995). In vivo characterization of phytochrome-phycocyanobilin adducts in yeast. J. Biol. Chem. 270: 20193-20200.
25. Kunkel, T., Tomizawa, K., Kern, R., Furuya, M., Chua, N.H., and Schäfer, E. (1993). In vitro formation of a photoreversible adduct of phycocyanobilin and tobacco apophytochrome B. Eur. J. Biochem. 215: 587-594.
26. Lapko, V.N., Jiang, X.Y., Smith, D.L., and Song, P.S. (1997). Posttranslational modification of oat phytochrome A: Phosphorylation of a specific serine in a multiple serine cluster. Biochemistry 36: 10595-10599.
27. Lapko, V.N., Jiang, X.Y., Smith, D.L., and Song, P.S. (1999). Mass spectrometric characterization of oat phytochrome A: Isoforms and posttranslational modifications. Protein Sci. 8: 1032-1044.
28. Lapko, V.N., Wells, T.A., and Song, P.S. (1996). Protein kinase Acatalyzed phosphorylation and its effect on conformation in phytochrome A. Biochemistry 35: 6585-6594.
29. Leivar, P., Monte, E., Al-Sady, B., Carle, C., Storer, A., Alonso, J.M., Ecker, J.R., and Quail, P.H. (2008). The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20: 337-352.
30. Mira-Rodado, V., Sweere, U., Grefen, C., Kunkel, T., Fejes, E., Nagy, F., Schäfer, E., and Harter, K. (2007). Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis. J. Exp. Bot. 58: 2595-2607.
31. Morelli, G., and Ruberti, I. (2002). Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci. 7: 399-404.
32. Nagy, F., and Schäfer, E. (2002). Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. Annu. Rev. Plant Biol. 53: 329-355.
33. Ni, M., Tepperman, J.M., and Quail, P.H. (1998). PIF3, a phytochromeinteracting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95: 657-667.
34. Oka, Y., Matsushita, T., Mochizuki, N., Suzuki, T., Tokutomi, S., and Nagatani, A. (2004). Functional analysis of a 450-amino acid N-terminal fragment of phytochrome B in Arabidopsis. Plant Cell 16: 2104-2116.
35. Pfeiffer, A., Nagel, M.K., Popp, C., Wüst, F., Bindics, J., Viczián, A., Hiltbrunner, A., Nagy, F., Kunkel, T., and Schäfer, E. (2012). Interaction with plant transcription factors can mediate nuclear import of phytochrome B. Proc. Natl. Acad. Sci. USA 109: 5892-5897.
36. Phee, B.K., Kim, J.I., Shin, D.H., Yoo, J., Park, K.J., Han, Y.J., Kwon, Y.K., Cho, M.H., Jeon, J.S., Bhoo, S.H., and Hahn, T.R. (2008). A novel protein phosphatase indirectly regulates phytochrome-interacting factor 3 via phytochrome. Biochem. J. 415: 247-255.
37. 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.
38. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17: 1030-1032.
39. Rockwell, N.C., Su, Y.S., and Lagarias, J.C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57: 837-858.
40. Ryu, J.S., et al. (2005). Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120: 395-406.
41. Saijo, Y., Zhu, D., Li, J., Rubio, V., Zhou, Z., Shen, Y., Hoecker, U., Wang, H., and Deng, X.W. (2008). Arabidopsis COP1/SPA1 complex and FHY1/FHY3 associate with distinct phosphorylated forms of phytochrome A in balancing light signaling. Mol. Cell 31: 607-613.
42. Shen, Y., Zhou, Z., Feng, S., Li, J., Tan-Wilson, A., Qu, L.J., Wang, H., and Deng, X.W. (2009). Phytochrome A mediates rapid red lightinduced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in a low fluence response. Plant Cell 21: 494-506.
43. Shimizu-Sato, S., Huq, E., Tepperman, J.M., and Quail, P.H. (2002). A light-switchable gene promoter system. Nat. Biotechnol. 20: 1041-1044.
44. Stockhaus, J., Nagatani, A., Halfter, U., Kay, S., Furuya, M., and Chua, N.H. (1992). Serine-to-alanine substitutions at the aminoterminal region of phytochrome A result in an increase in biological activity. Genes Dev. 6: 2364-2372.
45. Sweere, U., Eichenberg, K., Lohrmann, J., Mira-Rodado, V., Bäurle, 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.
46. Trupkin, S.A., Debrieux, D., Hiltbrunner, A., Fankhauser, C., and Casal, J.J. (2007). The serine-rich N-terminal region of Arabidopsis phytochrome A is required for protein stability. Plant Mol. Biol. 63: 669-678.
47. Van Buskirk, E.K., Decker, P.V., and Chen, M. (2012). Photobodies in light signaling. Plant Physiol. 158: 52-60.
48. Yang, S.W., Jang, I.-C., Henriques, R., and Chua, N.-H. (2009). FARRED ELONGATED HYPOCOTYL1 and FHY1-LIKE associate with the Arabidopsis transcription factors LAF1 and HFR1 to transmit phytochrome A signals for inhibition of hypocotyl elongation. Plant Cell 21: 1341-1359.
49. Yeh, K.C., and Lagarias, J.C. (1998). Eukaryotic phytochromes: Light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. USA 95: 13976-13981.
50. Yeh, K.C., Wu, S.H., Murphy, J.T., and Lagarias, J.C. (1997). A cyanobacterial phytochrome two-component light sensory system. Science 277: 1505-1508.