Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors

Biochemical Journal

Volumn 392, Issue 1, 2005, Pages 103-116

  Karniol, Baruch ^a,b   Wagner, Jeremiah R ^a   Walker, Joseph M ^a   Vierstra, Richard D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Bilin; Histidine kinase; Light perception; Phylogeny; Phytochrome

Indexed keywords

ACIDITY; BACTERIA; FUNGI; GENES; LIGHT ABSORPTION; MUTAGENESIS;

BILIN; HISTIDINE KINASE; LIGHT PERCEPTION; PHYLOGENY; PHYTOCHROME;

CHROMOPHORES;

ADENYLATE CYCLASE; CYSTEINE; LYASE; PHOSPHODIESTERASE; PHYTOCHROME;

ACIDITY; ACTINOBACTERIA; AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATOPHORE; CONTROLLED STUDY; CYANOBACTERIUM; ENZYME ACTIVITY; FUNGUS; KINEOCOCCUS RADIOTOLERANS; MICROBIAL ACTIVITY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPERON; PHYLOGENY; PHYTOCHROME; SEQUENCE HOMOLOGY, AMINO ACID;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); CYANOBACTERIA; FUNGI; KINEOCOCCUS RADIOTOLERANS;

EID: 27144507187     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20050826     Document Type: Article

References (54)

1. Briggs, W. R. and Spudich, J. L. (2005) Handbook of Photosensory Systems, Wiley-VCH Verlag GmbH & Co, Weinheim, Germany
2. Quail, P. H. (2002) Phytochrome photosensory signalling networks. Nat. Rev. Mol. Cell Biol. 3, 85-93
3. Smith, H. (2000) Phytochromes and light signal perception by plants - an emerging synthesis. Nature (London) 407, 585-591
4. Vierstra, R. D. (2002) Cyanophytochromes, bacteriophytochromes, and plant phytochromes: light-regulated kinases related to bacterial two-component regulators. In Histidine Kinases in Signal Transduction (Inouya, M. and Dutta, R., eds.), pp. 273-295, Academic Press, New York
5. Bhoo, S. H., Davis, S. J., Walker, J., Karniol, B. and Vierstra, R. D. (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature (London) 414, 776-779
6. Frankenberg, N., Mukougawa, K., Kohchi, T. and Lagarias, J. C. (2001) Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13, 965-978
7. Montgomery, B. L. and Lagarias, J. C. (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci. 7, 357-366
8. Wu, S. H. and Lagarias, J. C. (2000) Defining the bilin lyase domain: lessons from the extended phytochrome superfamily. Biochemistry 39, 13487-13495
9. Cherry, J. R., Hondred, D., Walker, J. M., Keller, J. M., Hershey, H. R 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
10. 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
11. Yeh, K. C. and Lagarias, J. C. (1998) Eukaryotic phytochromes - light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. U.S.A. 95, 13976-13981
12. Schneider-Poetsch, H. A. (1992) Signal transduction by phytochrome: phytochromes have a module related to the transmitter modules of bacterial sensor proteins. Photochem. Photobiol. 56, 839-846
13. Krall, L. and Reed, J. W. (2000) The histidine kinase-related domain participates in phytochrome B function but is dispensable. Proc. Natl. Acad. Sci. U.S.A. 97, 8169-8174
14. Matsushita, T., Mochizuki, N. and Nagatani, A. (2003) Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature (London) 424, 571-574
15. Marwan, W. and Starostzik, C. (2002) The sequence of regulatory events in the sporulation control network of Physarum polycephalum analysed by time-resolved somatic complementation of mutants. Protist 153, 391-400
16. Kehoe, D. M. and Grossman, A. R. (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science (Washington, D.C.) 273, 1409-1412
17. Yeh, K. C., Wu, S. H., Murphy, J. T. and Lagarias, J. C. (1997) A cyanobacterial phytochrome two-component light sensory system. Science (Washington, D.C.) 277, 1505-1508
18. Wilde, A., Churin, Y., Schubert, H. and Borner, T. (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett. 406, 89-92
19. Bhaya, D., Takahashi, A. and Grossman, A. R. (2001) Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proc. Natl. Acad. Sci. U.S.A. 98, 7540-7545
20. Park, C. M., Kim, J. I., Yang, S. S., Kang, J. G., Kang, J. H., Shim, J. Y., Chung, Y. H., Park, Y M. and Song, P. S. (2000) A second photochromic bacteriophytochrome from Synechocystis sp PCC 6803: spectral analysis and down-regulation by light. Biochemistry 39, 10840-10847
21. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gartner, W., Wilde, A. and Borner, T. (1997) A prokaryotic phytochrome. Nature (London) 386, 663
22. Davis, S. J., Vener, A. V. and Vierstra, R. D. (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science (Washington, D.C.) 286, 2517-2520
23. Catlett, N. L., Yoder, O. C. and Turgeon, B. G. (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell 2, 1151-1161
24. Lamparter, T., Michael, N., Mittmann, F. and Esteban, B. (2002) Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc. Natl. Acad. Sci. U.S.A. 99, 11628-11633
25. Karniol, B. and Vierstra, R. D. (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc. Natl. Acad. Sci. U.S.A. 100, 2807-2812
26. Lamparter, T., Michael, N., Caspani, O., Miyata, T., Shirai, K. and Inomata, K. (2003) Biliverdin binds covalently to Agrobacterium phytochrome Agp1 via its ring A vinyl side chain. J. Biol. Chem. 278, 33786-33792
27. Lamparter, T., Carrascal, M., Michael, N., Martinez, E., Rottwinkel, G. and Abian, J. (2004) The biliverdin chromophore binds covalently to a conserved cysteine residue in the N-terminus of Agrobacterium phytochrome Agp1. Biochemistry 43, 3659-3669
28. Wegele, R., Tasler, R., Zeng, Y. H., Rivera, M. and Frankenberg-Dinkel, N. (2004) The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. J. Biol. Chem. 279, 45791-45802
29. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D. Y., Paulsen, I., Nelson, K. E., Nelson, W. et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science (Washington, D.C.) 304, 66-74
30. Tyson, G. W., Chapman, J., Hugenholtz, P., Allen, E. E., Ram, R. J., Richardson, P. M., Solovyev, V. V., Rubin, E. M., Rokhsar, D. S. and Banfield, J. F. (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature (London) 428, 37-43
31. Aravind, L. and Ponting, C. P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22, 458-459
32. Giraud, E., Fardoux, J., Fourrier, N., Hannibal, L., Genty, B., Bouyer, P., Dreyfus, B. and Vermeglio, A. (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature (London) 417, 202-205
33. Herdman, M., Coursin, T., Rippka, R., Houmard, J. and Tandeau de Marsac, N. (2000) A new appraisal of the prokaryotic origin of eukaryotic phytochromes. J. Mol. Evol. 51, 205-213
34. Schmitz, O., Katayama, M., Williams, S. B., Kondo, T. and Golden, S. S. (2000) CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science (Washington, D.C.) 289, 765-768
35. Galperin, M. Y., Nikolskaya, A. N. and Koonin, E. V. (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203, 11-21
36. Fischer, A. J. and Lagarias, J. C. (2004) Harnessing phytochrome's glowing potential. Proc. Natl. Acad. Sci. U.S.A. 101, 17334-17339
37. Jorissen, H., Quest, B., Remberg, A., Coursin, T., Braslavsky, S. E., Schaffner, K., de Marsac, N. T. and Gartner, W. (2002) Two independent, light-sensing two-component systems in a filamentous cyanobacterium. Eur. J. Biochem. 269, 2662-2671
38. Bhoo, S. H., Hirano, T., Jeong, H. Y., Lee, J. G., Furuya, M. and Song, P. S. (1997) Phytochrome photochromism probed by site-directed mutations and chromophore esterification. J. Am. Chem. Soc. 119, 11717-11718
39. Talser, R., Moises, T. and Frankenberg-Dinkel, N. (2005) Biochemcial and spectroscopic characterization of the bacterial phytochrome of Pseudomonas aeroginosa. FEBS J. 272, 1927-1936
40. Karniol, B. and Vierstra, R. D. (2004) The HWE histidine kinases, a new family of bacterial two-component sensor kinases with potentially diverse roles in environmental signaling. J. Bacteriol. 186, 445-453
41. Inouye, M. and Dutta, R. (2003) Histidine Kinases in Signal Transmission, Academic Press, New York
42. Jorissen, H., Quest, B., Lindner, I., de Marsac, N. T. and Gartner, W. (2002) Phytochromes with noncovalently bound chromophores: The ability of apophytochromes to direct tetrapyrrole photoisomerization. Photochem. Photobiol. 75, 554-559
43. Zhao, K. H., Ran, Y., Li, M., Sun, Y. N., Zhou, M., Storf, M., Kupka, M., Bohm, S., Bubenzer, C. and Scheer, H. (2004) Photochromic biliproteins from the cyanobacterium Anabaena sp PCC 7120: Lyase activities, chromophore exchange, and photochromism in phytochrome AphA. Biochemistry 43, 11576-11588
44. Hanzawa, H., Shinomura, T., Inomata, K., Kakiuchi, T., Kinoshita, H., Wada, K. and Furuya, M. (2002) Structural requirement of bilin chromophore for the photosensory specificity of phytochromes A and B. Proc. Natl. Acad. Sci. U.S.A. 99, 4725-4729
45. 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. U.S.A. 98, 3612-3617
46. Seib, L. O. and Kehoe, D. M. (2002) A turquoise mutant genetically separates expression of genes encoding phycoerythrin and its associated linker peptides. J. Bacteriol. 184, 962-970
47. Aldridge, P., Paul, R., Goymer, P., Rainey, P. and Jenal, U. (2003) Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol. 47, 1695-1708
48. Huang, B. X., Whitchurch, C. B. and Mattick, J. S. (2003) FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 185, 7068-7076
49. Rashid, M. H., Rajanna, C., All, A. and Karaolis, D. K. R. (2003) Identification of genes involved in the switch between the smooth and rugose phenotypes of Vibrio cholerae. FEMS Microbiol. Lett. 227, 113-119
50. Lagarias, J. C. and Rapoport, H. (1980) Chromopeptides from phytochrome. The structure and linkage of the Pr form of the phytochrome chromophore. J. Am. Chem. Soc. 102, 4821-4829
51. Terauchi, K., Montgomery, B. L., Grossman, A. R., Lagarias, J. C. and Kehoe, D. M. (2004) RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol. Microbiol. 51, 567-577
52. Yoshihara, S., Katayama, M., Geng, X. X. and Ikeuchi, M. (2004) Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue- and green-absorbing forms. Plant Cell Physiol. 45, 1729-1737
53. Wilde, A., Fiedler, B. and Borner, T. (2002) The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol. Microbiol. 44, 981-988
54. Gong, W. M., Hao, B., Mansy, S. S., Gonzalez, G., Gilles-Gonzalez, M. A. and Chan, M. K. (1998) Structure of a biological oxygen sensor: A new mechanism for heme-driven signal transduction. Proc. Natl. Acad. Sci. U.S.A. 95, 15177-15182