Phosphorelay control of phycobilisome biogenesis during complementary chromatic adaptation

Photosynthesis Research

Volumn 53, Issue 2-3, 1997, Pages 95-108

  Grossman, Arthur R ^a   Kehoe, David M ^a  

^a GEOPHYSICAL LABORATORY   (United States)

Author keywords

Phosphorylation; Signal transduction; Two component regulation

Indexed keywords

CYANOBACTERIA;

EID: 0030817338     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/a:1005807221560     Document Type: Article

References (104)

1. Appleby JL, Parkinson JS and Bourret RB (1996) The multi-step phosphorelay: Not necessarily a road less traveled. Cell 86: 845-848
2. Bennett A and Bogorad L (1971) Properties of subunits and aggregates of blue-green algal biliproteins. Biochem 10: 3625-3634
3. Bennett A and Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58: 419-435
4. Bogorad L (1975) Phycobiliproteins and complementary chromatic adaptation. Annu Rev Plant Physiol 26: 369-401
5. Boyd JM and Lory S (1996) Dual function of PilS during transcriptional activation of the Pseudomonas aeruginosa pilin subunit gene. J Bacteriol 178: 831-839
6. Bruns B, Briggs WR and Grossman AR (1989) Molecular characterization of phycobilisome regulatory mutants in Fremyella diplosiphon. J Bacteriol 171: 901-908
7. Bryant DA (1981) The photoregulated expression of multiple phycocyanin species: General mechanism for control of phycocyanin synthesis in chromatically adapting cyanobacteria. Eur J Biochem 119:425-429
8. Bryant DA and Cohen-Bazire G (1981) Effects of chromatic illumination on cyanobacterial phycobilisomes: Evidence for the specific induction of a second pair of phycocyanin subunits in Pseudanabaena 7409 grown in red light. Eur J Biochem 119: 415-424
9. Burbulys D, Trach K and Hoch JA (1991) Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64: 545-552
10. Capuano V, Braux A-S, Tandeau de Marsac N and Houmard J (1991) The 'anchor polypeptide' of cyanobacterial phycobilisomes. Molecular characterization of the Synechococcus sp. PCC 6301 apcE gene. J Biol Chem 266: 7239-7247
11. Casey ES and Grossman AR (1994) In vivo and in vitro characterization of the light-regulated cpcB2A2 promoter of Fremyella diplosiphon. J Bacteriol 176: 6362-6374
12. Casey ES, Kehoe DM and Grossman AR (1997) Suppression of mutants aberrant in light intensity responses of complementary chromatic adaptation. J Bacteriol 179: 4599-4606
13. Cavicchioli R, Schroder I, Constanti M and Gunsalus RP (1995) The NarX and NarQ sensor-transmitter proteins of Escherichia coli each require two conserved histidines for nitrate-dependent signal transduction to NarL. J Bacteriol 177: 2416-2424
14. Chang C, Kwok SF, Bleecker AB and Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: Similarity of product to two-component regulators. Science 262: 539-544
15. Chiang GG, Schaefer MR and Grossman AR (1992) Complementation of a red-light indifferent cyanobacterial mutant. Proc Natl Acad Sci USA 89: 9415-9419
16. Clack T, Mathews S and Sharrock RA (1994) The phytochrome apoprotein family in Arabidopsis is encoded by five genes: The sequences and expression of PHYD and PHYE. Plant Mol Biol 25: 413-427
17. Clegg D and Koshland D (1984) The role of a signaling protein in bacterial sensing: Behavioral effects of increased gene expression. Proc Natl Acad Sci USA 81: 5056-5060
18. Cobley JG and Miranda RD (1983) Mutations affecting chromatic adaptation in the cyanobacterium Fremyella diplosiphon. J Bacteriol 153: 1486-1492
19. Cobley JG, Zerweck E, Reyes R, Mody A, Seludo-Unson JR, Jaeger H, Weerasuriya S and Navankasattusas S (1993) Construction of shuttle plasmids which can be efficiently mobilized from Escherichia coli into the chromatically adapting cyanobacterium Fremyella diplosiphon. Plasmid 30: 90-105
20. Collier JL and Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. Strain PCC 7942: not all bleaching is the same. J Bacteriol 174: 4718-4726
21. Collier JL and Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13: 1039-1047
22. Conley PB, Lemaux PG and Grossman AR (1985) Cyanobacterial light-harvesting complex subunits encoded in two red light-induced transcripts. Science 230: 550-553
23. Conley PB, Lemaux PG and Grossman AR (1988) Molecular characterization and evolution of sequences encoding light harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon. J Mol Biol 199: 447-465
24. Conley PB, Lemaux PG, LomaxTL and Grossman AR (1986) Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad Sci USA 83: 3924-3928
25. Diakoff S and Scheibe S (1973) Action spectra for chromatic adaptation in Tolypothrix. tenuis. Plant Physiol 51: 382-385
26. Engelmann TW (1883a) Farbe und Assimilation. Assimilation findet nur in den farbstoffhaltigen Plasmathielchen statt. II. Näherer Zusammenhang zwischen Lichtabsorption und Assimilation. Bot Z 41: 1-13
27. Engelmann TW (1883b) Farbe und Assimilation. III. Weitere Folgerungen. Bot Z 41: 17-29
28. Engelmann TW (1884) Untersuchungen über die qualitativen Beziehungen zwischen Absorption des Lichtes und Assimilation in Planzenzellen. I. Das Mikrospectrophotometer ein Apparat zur quantitativen Mikrospectralanalyse. II. Experimentelle Grundlagen zur Ermittelung der quantitativen Beziehungen zwischen Assimilationsenergie und Absorptionsgrösse. Bot Z 42: 97-105
29. Eraso JM and Kaplan S (1994) prrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol 176: 32-43
30. Fairchild CD and Glazer AN (1994) Oligomeric structure, enzyme kinetics, and substrate specificity of the phycocyanin α subunit phycocyanobilin lyase. J Biol Chem 269: 8686-8694
31. Fairchild CD, Zhao J, Zhou J, Colson SE, Bryant DA and Glazer AN (1992) Phycocyanin a-subunit phycocyanobilin lyase. Proc Natl Acad Sci USA 89: 7017-7021
32. Federspiel NA and Grossman AR (1990) Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bacteriol 172:4072-4081
33. Federspiel NA and Scott L (1992) Characterization of a light-regulated gene encoding a new phycoerythrin-associated linker protein from the cyanobacterium Fremyella diplosiphon. J Bacteriol 179: 5994-5998
34. Fiedler U and Weiss V (1995) A common switch in activation of the response regulators NtrC and PhoB: Phosphorylation induces dimerization of the receiver modules. EMBO J 14: 3696-3705
35. Fujita Y and Hattori A (1960a) Effect of chromatic lights on phycobilin formation in a blue-green alga. Tolypothrix tenuis. Plant Cell Physiol 1: 293-303
36. Fujita Y and Hattori A (1960b) Formation of phycoerythrin in preilluminated cells of Tolypothrix tenuis with special reference to nitrogen metabolism. Plant Cell Physiol 1: 281-292
37. Fujita Y and Hattori A (1962) Photochemical interconversion between precursors of phycobilin chromoproteids in Tolypothrix tenuis. Plant Cell Physiol 3: 209-220
38. Gaidukov N (1903) Die Farbervänderung bei den Prozessen der Komplementären chromatischen Adaptation. Berichte der Deutschen Botanischen Gesellschaft 21: 517-522
39. Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32: 327-347
40. Glazer AN (1982) Phycobilisomes: structure and dynamics. Ann Rev of Microbiol 36: 173-198
41. Glazer AN (1985) Light harvesting by phycobilisomes. Ann Rev of Biophys and Biophys Chem 14: 47-77
42. Glazer AN, Lundell DJ, Yamanaka G and Williams RC (1983) The structure of a 'simple' phycobilisome. Annals Institut Pasteur/Microbiology 134B:159-180
43. Groisman EA, Chiao E, Lipps CJ and Heffron F (1989) Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci USA 86: 7077-7081
44. Grossman AR (1990) Chromatic adaptation and the events involved in phycobilisome biosynthesis. Plant Cell Environ 13: 651-666
45. Grossman AR, Bhaya D, Apt KE and Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: Diversity, control and evolution. Annu Rev Genet 29: 231-287
46. Grossman AR, Schaefer M, Chiang G and Collier J (1994) The responses of cyanobacteria to environmental conditions: Light and nutrients. In Bryant D (ed) The Molecular Biology of Cyanobacteria, pp 641-675. Kluwer Academic Publishers, Dordrecht, the Netherlands
47. Grossman AR, Schaefer MR, Chiang GG and Collier JL (1993) The phycobilisome: A light harvesting complex responsive to environmental conditions. Microbiol Rev 57: 725-749
48. Hattori A and Fujita Y (1959a) Formation of phycobilin pigments in a blue-green alga, Tolypothrix tenuis, as induced by illumination with colored lights. J Biochem 46: 521-524
49. Hattori A and Fujita Y (1959b) Effect of pre-illumination on the formation of phycobilin pigments in a blue-green alga, Tolypothrix tenuis. J Biochem 46: 159-1261
50. Haury JF and Bogorad L (1977) Action spectra for phycobiliprotein synthesis in a chromatically adapting cyanophyte, Fremyella diplosiphon. Plant Physiol 60: 835-839
51. Hertig C, Li RY, Louarn A-M, Garnerone A-M, David M, Batut J, Kahn D and Boistard P (1989) Rhizobium meliloti regulatory gene fixJ activates transcription of R. meliloti nifA and fixK Genes in Escherichia coli. J Bacteriol 171: 1736-1738
52. Hiller RG, Anderson JM and Larkum AWD (1991) The chlorophyll-protein complexes of algae. In: Scheer H (ed) Chlorophylls, pp 529-547. CRC Press, Boca Raton, FL
53. Hofmann E, Wrench PM, Sharples FP, Hiller RG, Welte W and Diederichs K (1996) Structural basis of light harvesting by carotenoids: Peridinin-chlorophyll-protein from Amphidinium carterae. Science 272: 1788-1791
54. Houmard J, Capuano V, Cousin T and Tandeau de Marsac N (1988) Genes encoding core components of the phycobilisome in the cyanobacterium Calothrix sp. strain 7601. Occurrence of a multigene family. J Bacteriol 170: 5512-5521
55. Hua J, Chang C, Sun Q and Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269: 1712-1714
56. Ishige K, Nagasawa S, Tokishita S-I and Mizuno T (1994) A novel device of bacterial signal transducers. EMBO J 13: 5195-5202
57. Jacobs JD, Ludwig JR, Hildebrand M, Kukel A, Feng T-Y, Ord RW and Volcani BE (1992) Characterization of two circular plasmids from the marine diatom Cylindrothece fusiformis: Plasmids hybridize to chloroplast and nuclear DNA. Mol Gen Genet 233: 302-310
58. Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184: 1-19
59. Kahn K and Schaefer MR (1995) Characterization of transposon Tn5469 from the cyanobacterium Fremyella diplosiphon. J Bacteriol 177: 7026-7032
60. Kehoe DM and Grossman AR (1994) Complementary chromatic adaptation: Photoperception to gene regulation. Sem in Cell Biol 5:303-313
61. Kehoe DM and Grossman AR (1995) The use of site directed mutagenesis in the analysis of complementary chromatic adaptation. In: Proceedings from the Xth International Photosynthesis Congress: Photosynthesis: From Light to Biosphere. Kluwer Academic Publishers, Dordrecht, the Netherlands
62. Kehoe DM and Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409-1412
63. Kehoe DM and Grossman AR (1997) New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J Bacteriol (in press)
64. Kendrick RE and Kronenberg GHM (1994) Photomorphogenesis in Plants. 2nd ed. Kluwer Academic Publishers, Dordrecht, the Netherlands
65. Klose KE, Weiss DS and Kustu S (1993) Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J Mol Biol 232: 67-78
66. Lee T-Y, Makino K, Shinagawa H, Amemura M and Nakata A (1989) Phosphate regulon in members of the family Enterobacteriaceae: Comparison of the phoB-phoR operons of Escherichia coli, Shigella dysenteriae, and Klebsiella pneumoniae. J Bacteriol 171: 6593-6599
67. Lomax TL, Conley PB, Schilling J and Grossman AR (1987) Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA. J Bacteriol 169: 2675-2684
68. Lukat GS, McCleary WR, Stock AM and Stock JB (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci USA 89: 718-722
69. Mazel D and Marliere P (1989) Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature 341: 245-248
70. Mazel D, Bernard C, Schwarz R and Tandeau de Marsac N (1991) Characterization of two insertion sequences from the cyanobacterium Calothrix sp. PCC 7601. Mol Microbiol 5: 2165-2170
71. Mazel D, Guglielmi G, Houmard H, Sidler W, Bryant DA and Tandeau de Marsac N (1986) Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res 14: 8279-8290
72. Mazel D, Houmard J and Tandeau de Marsac N (1988) A multigene family in Calothrix sp. PCC 7601 encodes phycocyanin, the major component of the cyanobacterial light-harvesting antenna. Mol Gen Genet 211: 296-304
73. Melchers LS, Thompson DV, Idler KB, Schilperoort RA and Hooykaas PJ (1986) Nucleotide sequence of the virulence gene virG of the Agrobacterium tumefaciens octopine Ti plasmid: Significant homology between virG and the regulatory genes ompR, phoB and dye of E. coli. Nucleic Acids Res 14: 9933-9942
74. Mettke I, Fiedler U and Weiss V (1995) Mechanism of activation of a response regulator: Interaction of NtrC-P dimers induces ATPase activity. J Bacteriol 177: 5056-5061
75. Oelmüller R, Conley PB, Federspiel N, Briggs WR and Grossman AR (1988a) Changes in accumulation and synthesis of transcripts encoding phycobilisome components during acclimation of Fremyella diplosiphon to different light qualities. Plant Physiol 88: 1077-1083
76. Oelmüller R, Grossman AR and Briggs WR (1988b) Photoreversibility of the effect of red and green light pulses on the accumulation in darkness of mRNAs coding for phycocyanin and phycoerythrin in Fremyella diplosiphon. Plant Physiol 88: 1084-1091
77. Parkinson JS and Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26: 71-112
78. Perego M and Hoch JA (1991) Negative regulation of Bacillus subtilis sporulation by spoOE gene product. J Bacteriol 173: 2514-2520
79. Perego M and Hoch JA (1996) Protein aspartate phosphatases control the output of two-component signal transduction systems. Trends Genet 12: 97-101
80. Porter G, Tredwell CJ, Searle GFW and Barber J (1978) Picosecond time-resolved energy transfer in Porphyridium cruentum. Part I. In the intact alga. Biochim Biophys Acta 501: 232-245
81. Posas R, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC and Saito H (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 'two-component' osmosensor. Cell 86: 865-875
82. Ravid S, Matsumura P and Eisenbach M (1986) Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the chemotaxis protein CheY Proc Natl Acad Sci USA 83: 7157-7161
83. Rogowsky PM, Close TJ, Chimera JA, Shaw JJ and Kado CI (1987) Regulation of the vir Genes of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol 169: 5101-5112
84. Schmidt-Goff CM and Federspiel NA (1993) In vivo and in vitro footprinting of a light-regulated promoter in the cyanobacterium Fremyella diplosiphon. J Bacteriol 175: 1806-1813
85. Schneider-Poetsch HAW, Braun B, Marx S and Schaumburg A (1991) Phytochromes and bacterial sensor proteins are related by structural and functional homologies. FEBS Lett 281: 245-249
86. Searle GFW, Barber J, Porter G and Tredwell CJ (1978) Picosecond time-resolved energy transfer in Porphyridium cruentum. Part II. In the isolated light-harvesting complex (phycobilisomes). Biochim Biophys Acta 501: 246-256
87. Seki T, Yoshikawa H, Takahashi H and Saito H (1988) Nucleotide sequence of the Bacillus subtilis phoR gene. J Bacteriol 170: 5935-5938
88. Shattuck-Eidens DM and Kadner RJ (1983) Molecular cloning of the uhp region and evidence for a positive activator for expression of the hexose phosphate transport system of Escherichia coli. J Bacteriol 155: 1062-1070
89. Sidler WA (1994) Phycobilisome and phycobiliprotein structures. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 139-216. Kluwer Academic Publishers, Dordrecht, the Netherlands
90. Sobczyk A, Bely A, Tandeau de Marsac N and Houmard J (1994) A phosphorylated DNA-binding protein is specific for the red-light signal during complementary chromatic adaptation in cyanobacteria. Mol Microbiol 13: 875-885
91. Sobczyk A, Schyns G, Tandeau de Marsac N and Houmard J (1993) Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix sp. PCC 7601: DNA-binding proteins and modulation by phosphorylation. EMBO J 12: 997-1004
92. Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130: 82-91
93. Tandeau de Marsac N (1983) Phycobilisomes and complementary adaptation in cyanobacteria. Bulletin de L'Institut Pasteur 81: 201-254
94. Tandeau de Marsac N and Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: New steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119-190
95. Thümmler F, Algorra P and Fobo GM (1995) Sequence similarities of phytochrome to protein kinases: Implication for the structure, function and evolution of the phytochrome gene family. FEBS Lett 357: 149-155
96. Uhl MA and Miller JF (1996) Integration of multiple domains in a two-component sensor protein: The Bordetella pertussis BvgAS phosphorelay. EMBO J 15(5): 1028-1036
97. Vogelmann TC and Scheibe J (1978) Action spectrum for chromatic adaptation in the blue-green alga Fremyella diplosiphon. Planta 143: 233-239
98. Wanner BL (1994) Phosphate-regulated genes for the utilization of phosphonates in members of the family Enterobacteriaceae. In Torriani-Gorini A, Yagil E and Silver S (ed) Phosphate in Microorganisms. Cellular and Molecular Biology, pp 215-222. ASM Press, Washington, DC
99. Wanner BL and Wilmes-Riesenberg MR (1992) Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in the control of the phosphate regulation in an Escherichia coli. J Bacteriol 174: 2124-2130
100. Wilkinson JQ, Lanahan MB, Yen H-C, Giovannoni JJ and Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by Never-ripe. Science 270: 1807-1809
101. Wolfe AJ, Conley P, Kramer TJ and Berg HC (1987) Reconstitution of signaling in bacterial chemotaxis. J Bacteriol 169: 1878-1885
102. Wurtzel ET, Chou MY and Inouye M (1982) Osmoregulation of gene expression. I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem 257: 13685-13691
103. Yamaguchi S, Aizawa S-I, Kihara M, Isomura M, Jones CJ and Macnab RM (1986) Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol 168: 1172-1179
104. Yamanaka G and Glazer AN (1980) Dynamic aspects of phycobilisome structure. Phycobilisome turnover during nitrogen starvation in Synechococcus sp. Arch Microbiol 124: 39-47