Functional analysis of a 450-amino acid N-terminal fragment of phytochrome B in Arabidopsis

Plant Cell

Volumn 16, Issue 8, 2004, Pages 2104-2116

  Oka, Yoshito ^a   Matsushita, Tomonao ^a   Mochizuki, Nobuyoshi ^a   Suzuki, Tomomi ^a   Tokutomi, Satoru ^b   Nagatani, Akira ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; PHOTOSYNTHESIS; PLANT CELL CULTURE; SPECTRUM ANALYSIS;

FUNCTIONAL ANALYSIS; NUCLEAR LOCALIZATION SIGNAL; PHYTOCHROMES;

AMINO ACIDS;

AMINO ACIDS; CELLS; ENZYMES; PHOTORECEPTORS; PHOTOSYNTHESIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 4043083523     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.022350     Document Type: Article

References (69)

1. Andel, F., 3rd, Lagarias, J.C., and Mathies, R.A. (1996). Resonance Raman analysis of chromophore structure in the lumi-R photoproduct of phytochrome. Biochemistry 35, 15997-16008.
2. Aukerman, M.J., Hirschfeld, M., Wester, L., Weaver, M., Clack, T., Amasino, R.M., and Sharrock, R.A. (1997). A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 9, 1317-1326.
3. Bauer, D., Viczian, A., Kircher, S., Nobis, T., Nitschke, R., Kunkel, T., Panigrahi, K.C.S., Adam, E., Fejes, E., Schafer, 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.
4. Berkelman, T.R., and Lagarias, J.C. (1986). Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal. Biochem. 156, 194-201.
5. Boylan, M., Douglas, N., and Quail, P.H. (1994). Dominant negative suppression of Arabidopsis photoresponses by mutant phytochrome A sequences identifies spatially discrete regulatory domains in the photoreceptor. Plant Cell 6, 449-460.
6. Boylan, M.T., and Quail, P.H. (1991). Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc. Natl. Acad. Sci. USA 88, 10806-10810.
7. Briggs, W.R., and Christie, J.M. (2002). Phototropins 1 and 2: Versatile plant blue-light receptors. Trends Plant Sci. 7, 204-210.
8. Briggs, W.R., and Huala, E. (1999). Blue-light photoreceptors in higher plants. Annu. Rev. Cell Dev. Biol. 15, 33-62.
9. Casal, J.J. (1996). Phytochrome A enhances the promotion of hypocotyls growth caused by reductions in levels of phytochrome B in its FR-light-absorbing form in light-grown Arabidopsis thatiana. Plant Physiol. 112, 965-973.
10. 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.
11. Cherry, J.R., Hondred, D., Walker, J.M., Keller, J.M., Hershey, H.P., and Vierstra, R.D. (1993). Carboxy-terminal deletion analysis of oat phytochrome A reveals the presence of separate domains required for structure and biological activity. Plant Cell 5, 565-575.
12. 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.
13. 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.
14. Devlin, P.F., Patel, S.R., and Whitelam, G.C. (1998). Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 10, 1479-1488.
15. Eichenberg, K., Baurle, I., Paulo, N., Sharrock, R.A., Rudiger, W., and Schafer, E. (2000). Arabidopsis phytochromes C and E have different spectral characteristics from those of phytochromes A and B. FEBS Lett. 470, 107-112.
16. Eichenberg, K., Kunkel, T., Kretsch, T., Speth, V., and Schafer, E. (1999). In vivo characterization of chimeric phytochromes in yeast. J. Biol. Chem. 274, 354-359.
17. Elich, T.D., and Chory, J. (1997). Biochemical characterization of Arabidopsis wild type and mutant phytochrome B holoproteins. Plant Cell 9, 2271-2280.
18. Fankhauser, C., Yeh, K.C., Lagarias, J.C., Zhang, H., Elich, T.D., and Chory, J. (1999). PKS1, a substrate phosphorylated-byphytochromes that modulates light signaling in Arabidopsis. Science 284, 1539-1541.
19. Franklin, K.A., Davis, S.J., Stoddart, W.M., Vierstra, R.D., and Whitelam, G.C. (2003). Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell 15, 1981-1989.
20. Fu, E., Friedman, L., and Siegelman, H.W. (1979). Mass-spectral identification and purification of phycoerythrobilin and phycocyanobilin. Biochem. J. 179, 1-6.
21. Furuya, M. (1993). Phytochromes: Their molecular species, gene families, and functions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 617-645.
22. Furuya, M., and Song, P.S. (1994). Assembly and properties of holophytochrome. In Photomorphogenesis in Higher Plants, 2nd ed., R.E. Kendrick and G.H.M. Kronenberg, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 105-140.
23. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994.
24. Hanzawa, H., Inomata, K., Kinoshita, H., Kakiuchi, T., Jayasundera, K.P., Sawamoto, D., Ohta, A., Uchida, K., Wada, K., and Furuya, M. (2001). In vitro assembly of phytochrome B apoprotein with synthetic analogs of the phytochrome chromophore. Proc. Natl. Acad. Sci. USA 98, 3612-3617.
25. Hisada, A., Hanzawa, H., Weller, J.L., Nagatani, A., Reid, J.B., and Furuya, M. (2000). Light-induced nuclear translocation of endogenous pea phytochrome A visualized by immunocytochemical procedures. Plant Cell 12, 1063-1078.
26. Huq, E., and Quail, P.H. (2002). PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21, 2441-2450.
27. Jarillo, J.A., Capel, J., Tang, R.H., Yang, H.Q., Alonso, J.M., Ecker, J.R., and Cashmore, A.R. (2001). An Arabidopsis circadian clock component interacts with both CRY1 and phyB. Nature 410, 487-490.
28. Kay, S. (1997). PAS, present and future: Clues to the origin of circadian clocks. Science 276, 753-754.
29. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003). Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15, 2399-2407.
30. Kircher, S., Gil, P., Kozma-Bognar, L., Fejes, E., Speth, V., Husselstein-Muller, T., Bauer, D., Kim, L., Adam, E., Schafer, E., and Nagy, F. (2002). 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, 1541-1555.
31. Kircher, S., Kozma-Bognar, L., Kim, L., Adam, E., Harter, K., Schafer, E., and Nagy, F. (1999). Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11, 1445-1456.
32. Krall, L., and Reed, J.W. (2000). The histidine kinase-related domain participates in phytochrome B function but is dispensable. Proc. Natl. Acad. Sci. USA 97, 8169-8174.
33. Kretsch, T., Poppe, C., and Schafer, 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.
34. Lagarias, J.C., and Lagarias, D.M. (1989). Self-assembly of synthetic phytochrome holoprotein in vitro. Proc. Natl. Acad. Sci. USA 86, 5778-5780.
35. Li, L., and Lagarias, J.C. (1992). Phytochrome assembly. Defining chromophore structural requirements for covalent attachment and photoreversibility. J. Biol. Chem. 260, 2415-2423.
36. Liu, X.L., Covington, M.F., Fankhauser, C., Chory, J., and Wagner, D.R. (2001). ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293-1304.
37. Mancinelli, A.L. (1994). The physiology of phytochrome action. In Photomorphogenesis in Higher Plants, 2nd ed., R.E. Kendrick and G.H.M. Kronenberg, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 211-269.
38. Martinez-Garcia, J.F., Huq, E., and Quail, P.H. (2000). Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859-863.
39. Mathews, S., and Sharrock, R.A. (1997). Phytochrome gene diversity. Plant Cell Environ. 20, 666-671.
40. Matsushita, T., Mochizuki, N., and Nagatani, A. (2003). Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424, 571-574.
41. McCormac, A.C., Wagner, D., Boylan, M.T., Quail, P.H., Smith, H., and Whitelam, G.C. (1993). Photoresponses of transgenic Arabidopsis seedlings expressing introduced phytochrome B-encoding cDNAs: Evidence that phytochrome A and phytochrome B have distinct photoregulatory functions. Plant J. 4, 19-27.
42. Mochizuki, N., Brusslan, J.A., Larkin, R., Nagatani, A., and Chory, J. (2001). Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl. Acad. Sci. USA 98, 2053-2058.
43. Monte, E., Alonso, J.M., Ecker, J.R., Zhang, Y., Li, X., Young, J., Austin-Phillips, S., and Quail, P.H. (2003). Isolation and characterization of phyC mutants in Arabidopsis reveals complex cross talk between phytochrome signaling pathways. Plant Cell 15, 1962-1980.
44. Montgomery, B.L., and Lagarias, J.C. (2002). Phytochrome ancestry: Sensors of bilins and light. Trends Plant Sci. 7, 357-366.
45. Nagatani, A., Reed, J.W., and Chory, J. (1993). Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol. 102, 269-277.
46. Neff, M.M., Fankhauser, C., and Chory, J. (2000). Light: An indicator of time and place. Genes Dev. 14, 257-271.
47. Ni, M., Tepperman, J.M., and Quail, P.H. (1998). PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95, 657-667.
48. Ni, M., Tepperman, J.M., and Quail, P.H. (1999). Binding of phytochrome B to its nuclear signaling partner PIF3 is reversibly induced by light. Nature 400, 781-784.
49. Quail, P.H. (1997). An emerging molecular map of the phytochromes. Plant Cell Environ. 20, 657-665.
50. Quail, P.H., Boylan, M.T., Parks, B.M., Short, T.W., Xu, Y., and Wagner, D. (1995). Phytochromes: Photosensory perception and signal transduction. Science 268, 675-680.
51. 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.
52. Reiff, U., Eilfeld, O., and Rudiger, W. (1985). A photoreversible 39-kDalton fragment from the Pfr form of 124-kDalton phytochrome. Z. Naturforsch. 40, 693-698.
53. Robson, P.R.H., Whitelam, G.C., and Smith, H. (1993). Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants of Arabidopsis thaliana and Brassica napa deficient in phytochrome B. Plant Physiol. 102, 1179-1184.
54. Sakamoto, K., and Nagatani, A. (1996). Nuclear localization activity of phytochrome B. Plant J. 10, 859-868.
55. Schafer, E., and Bowler, C. (2002). Phytochrome-mediated photoperception and signal transduction in higher plants. EMBO Rep. 3, 1042-1048.
56. Schneider-Poetsch, H.A.W. (1992). Signal transduction by phytochrome: Phytochromes have a module related to the transmitter modules of bacterial sensor proteins. Photochem. Photobiol. 56, 839-846.
57. Shimizu-Sato, S., Huq, E., Tepperman, J.M., and Quail, P.H. (2002). A light-switchable gene promoter system. Nat. Biotechnol. 10, 1041-1044.
58. Shinomura, T., Nagatani, A., Kanzawa, 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.
59. Shinomura, T., Uchida, K., and Furuya, M. (2001). Elementary processes of photoperception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiol. 122, 147-156.
60. Smith, H., and Whitelam, G.C. (1997). The shade avoidance syndrome: Multiple responses mediated by multiple phytochromes. Plant Cell Environ. 20, 840-844.
61. Stockhaus, J., Nagatani, A., Halfter, U., Kay, S., Furuya, M., and Chua, N.H. (1992). Serine-to-alanine substitutions at the amino-terminal region of phytochrome A result in an increase in biological activity. Genes Dev. 6, 2364-2372.
62. Sweere, U., Eichenberg, K., Lohrmann, J., Mira-Rodado, V., Baurle, I., Kudla, J., Nagy, F., Dchafer, E., and Harter, K. (2001). Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294, 1108-1111.
63. 2-terminal domains of phytochromes A and B determine their photosensory specificity and differential light lability. Proc. Natl. Acad. Sci. USA 93, 4011-4015.
64. Wagner, D., Koloszvari, M., and Quail, P.H. (1996a). Two small spatially distinct regions of phytochrome B are required for efficient signaling rates. Plant Cell 8, 859-871.
65. Wu, S.-H., and Lagarias, J.C. (2000). Defining the bilin lyase domain: Lessons from the extended phytochrome superfamily. Biochemistry 39, 13487-13495.
66. Yamaguchi, R., Nakamura, M., Mochizuki, N., Kay, S.A., and Nagatani, A. (1999). Light-dependent translocation of a phytochrome B:GFP fusion protein to the nucleus in transgenic Arabidopsis. J. Cell Biol. 145, 437-445.
67. Yamamoto, K.T., and Furuya, M. (1983). Spectral properties of chromophore-containing fragments prepared from pea phytochrome by limited proteolysis. Plant Cell Physiol. 24, 713-718.
68. 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.
69. Zhu, Y., Tepperman, J.M., Fairchild, C.D., and Quail, P.H. (2000). Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix-loop-helix factor PIF3 in a reaction requiring the PAS domain of PIF3. Proc. Natl. Acad. Sci. USA 97, 13419-13424.