Responding to color: The regulation of complementary chromatic adaptation

Annual Review of Plant Biology

Volumn 57, Issue , 2006, Pages 127-150

  Kehoe, David M ^a   Gutu, Andrian ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Cyanobacteria; Light harvesting; Light regulation; Phytochrome photoreceptors; Redox regulation; Signal transduction

Indexed keywords

ADAPTATION; COLOR; CYANOBACTERIUM; PHOTOSYNTHESIS; PHYSIOLOGY; REVIEW;

ADAPTATION, PHYSIOLOGICAL; COLOR; CYANOBACTERIA; PHOTOSYNTHESIS;

CYANOBACTERIA;

EID: 33745939901     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.57.032905.105215     Document Type: Review

References (113)

1. Alvey RM, Karty JA, Roos E, Reilly JP, Kehoe DM. 2003. Lesions in phycoerythrin chromophore biosynthesis in Fremyella diplosiphon reveal coordinated light regulation of apoprotein and pigment biosynthetic enzyme gene expression. Plant Cell 15:2448-63
2. Appleby JL, Parkinson JS, Bourret RB. 1996. Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86:845-48
3. Atkinson MR, Ninfa AJ. 1993. Mutational analysis of the bacterial signal-transducing protein kinase/phosphatase nitrogen regulator II (NRII or NtrB). J. Bacteriol. 175:7016-23
4. Balabas BE, Montgomery BL, Ong LE, Kehoe DM. 2003. CotB is essential for complete activation of green light-induced genes during complementary chromatic adaptation in Fremyella diplosiphon. Mol. Microbiol. 50:781-93
5. Beale SI. 1993. Biosynthesis of phycobilins. Chem. Rev. 93:785-802
6. Beguin S, Guglielmi G, Rippka R, Cohen-Bazire G. 1985. Chromatic adaptation in a mutant of Fremyella diplosiphon incapable of phycoerythrin synthesis. Biochimie 67:109-17
7. Bennett A, Bogorad L. 1973. Complementary chromatic adaptation in a filamentous blue-green alga. J. Cell. Biol. 58:419-35
8. Bogorad L. 1975. Phycobiliproteins and complementary chromatic adaptation. Annu. Rev. Plant Physiol. 26:369-401
9. Bogorad L, Gendel SM, Haury JF, Koller K-P. 1982. Photomorphogenesis and complementary chromatic adaptation in Fremyella diplosyphon. In Proceedings of the Special FEBS Meeting on Cell Function and Differrentiation, ed. GC Papageorgiou, L Packer, pp. 119-26. Athens, Greece, April 25-29
10. Boresch K. 1922. Die komplementäre chromatic Adaptation. Arch. Protistenkd. 44:1-70
11. Bruns BU, Briggs WR, Grossman AR. 1989. Molecular characterization of phycobilisome regulatory mutants of Fremyella diplosiphon. J. Bacteriol. 171:901-8
12. Bryant DA. 1982. Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. J. Gen. Microbiol. 128:835-44
13. Bryant DA, Guglielmi G, Tandeau de Marsac N, Castets AM, Cohen-Bazire G. 1979. The structure of cyanobacterial phycobilisomes: a model. Arch. Microbiol. 123:113-27
14. Buchanan BB, Balmer Y. 2005. Redox regulation: a broadening horizon. Annu. Rev. Plant. Biol. 56:187-220
15. Cai YP, Wolk CP. 1990. Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J. Bacteriol. 172:3138-45
16. Campbell D. 1996. Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142:1255-63
17. Campbell D, Houmard J, Tandeau de Marsac N. 1993. Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix. Plant Cell 5:451-63
18. Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G. 1998. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol. Mol. Biol. Rev. 62:667-83
19. Casey ES, Grossman AR. 1994. In vivo and in vitro characterization of the light-regulated cpcB2A2 promoter of Fremyella diplosiphon. J. Bacteriol. 176:6362-74
20. Cavicchioli R, Schroder I, Constanti M, 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. 177:2416-24
21. Chiang GG, Schaefer MR, Grossman AR. 1992. Complementation of a red-light-indifferent cyanobacterial mutant. Proc. Natl. Acad. Sci. USA 89:9415-19
22. Chiang GG, Schaefer MR, Grossman AR. 1992. Transformation of the filamentous cyanobacterium Fremyella diplosiphon by conjugation or electroporation. Plant Physiol. Biochem. 30:315-25
23. Cobley JG, Clark AC, Weerasurya S, Queseda FA, Xiao JY, et al. 2002. CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol. Microbiol. 44:1517-31
24. Cobley JG, Miranda RD. 1983. Mutations affecting chromatic adaptation in the cyanobacterium Fremyella diplosiphon. J. Bacteriol. 153:1486-92
25. Cobley JG, Seneviratne L, Drong L, Thounaojam M, Oda JF, Carroll J. 1999. Transposition of Tn5 derivatives in the chromatically adapting cyanobacterium, Fremyella diplosiphon. In The Phototrophic Prokaryotes, ed. G Peschek, W Löffelhardt, G Schmetterer, pp. 443-51. New York: Kluwer Acad./Plenum
26. Cobley JG, Zerweck E, Reyes R, Mody A, Seludo-Unson JR, et al. 1993. Construction of shuttle plasmids which can be efficiently mobilized from Escherichia coli into the chromatically adapting cyanobacterium, Fremyella diplosiphon. Plasmid 30:90-105
27. Conley PB, Lemaux PG, Grossman AR. 1988. Molecular characterization and evolution of sequences encoding light-harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon. J. Mol. Biol. 199:447-65
28. Conley PB, Lemaux PG, Grossman AR. 1985. Cyanobacterial light-harvesting complex subunits encoded in two red-light induced transcripts. Science 230:550-53
29. Conley PB, Lemaux PG, Lomax TL, Grossman AR. 1986. Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc. Natl. Acad. Sci. USA 83:3924-28
30. Crossett RN, Drew EA, Larkum AWD. 1965. Chromatic adaptation in benthic marine algae. Nature 207:547-48
31. Csiszar K, Houmard J, Damerval T, Tandeau de Marsac N. 1987. Transcriptional analysis of the cyanobacterial gvpABC operon in differentiated cells: occurrence of an antisense RNA complementary to three overlapping transcripts. Gene 60:29-37
32. Damerval T, Guglielmi G, Houmard J, Tandeau de Marsac N. 1991. Hormogonium differentiation in the cyanobacterium Calothrix - a photoregulated developmental process. Plant Cell 3:191-201
33. Damerval T, Houmard J, Guglielmi G, Csiszar K, Tandeau de Marsac N. 1987. A developmentally regulated gvpABC operon is involved in the formation of gas vesicles in the cyanobacterium Calothrix 7601. Gene 54:83-92
34. Diakoff S, Scheibe J. 1975. Cultivation in the dark of blue-green alga Fremyella diplosiphon. A photo reversible effect of green and red light on growth rate. Physiol. Plant. 34:125-28
35. Diakoff S, Scheibe J. 1973. Action spectra for chromatic adaptation in Tolypothrix tennis. Plant Physiol. 51:382-85
36. Engelmann TW. 1902. Untersuchungen über die qualitativen Beziehungen zwieschen Absorbtion des Lichtes und Assimilation in Pflanzenzellen. I. Das Mikrospectraphotometer, ein Apparat zur qualitativen Mikrospectralanalyse. II. Experimentelle Grundlangen zur Ermittelung der quantitativen Beziehungen zwieschen Assimilationsenergie und Absorptiongrösse. III. Bestimmung der Vertheilung der Energie im Spectrum von Sonnenlicht mittels Bacterien-methode und quantitativen Mikrospectralanalyse. Bot. Z. 42:81-105
37. Engelmann TW. 1883. Farbe und Assimilation. I. Assimilation findet nur in den farbstoffhaltigen Plasmatheilchen statt. II Näherer Zusammenhang zwischen Lichtabsorbtion und Assimilation. III. Weitere folgerungen. Bot. Z. 41:1-29
38. Fauchon M, Lagniel G, Aude JC, Lombardia L, Soularue P, et al. 2002. Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell. 9:713-23
39. Federspiel NA, Grossman AR. 1990. Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J. Bacteriol. 172:4072-81
40. Federspiel NA, Scott L. 1992. Characterization of a light-regulated gene encoding a new phycoerythrin-associated linker protein from the cyanobacterium Fremyella diplosiphon. J. Bacteriol. 174:5994-98
41. Deleted in proof
42. Frankenberg N, Mukougawa K, Kohchi T, Lagarias JC. 2001. Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13:965-78
43. Fujita Y, Bauer CE. 2003. The light-independent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In The Porphyrin Handbook, Vol. 13, ed. KM Kadish, KM Smith, R Guilard, pp. 109-56. San Diego, CA: Elsevier Sci.
44. Fujita Y, Hattori A. 1960. Effect of chromatic lights on phycobilin formation in a blue-green alga, Tolypothrix tennis. Plant Cell Physiol. 1:293-303
45. Fujita Y, Hattori A. 1960. Formation of phycoerythrin in pre-illuminated cells of Tolypothrix tennis with special reference to nitrogen metabolism. Plant Cell Physiol. 1:281-92
46. Fujita Y, Hattori A. 1962. Photochemical interconversion between precursors of phycobilin chromoproteids in Tolypothrix tennis. Plant Cell Physiol. 3:209-20
47. Gaiducov N. 1903. Die Farben Veränderung bei den Prozessen der komplementären chromatischen Adaptation. Ber. Deutsch. Bot. Ges. 21:517-22
48. Gaiducov N. 1902. Über den Einfluss farbigen Lichtes auf die Färbung lebender Oscillarien. Abh. Preuss. Akad. Wiss. 5:1-36
49. Gantt E. 1981. Phycobilisomes. Annu. Rev. Plant Physiol. 32:327-47
50. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. 2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31:3784-88
51. Gendel S, Ohad I, Bogorad L. 1979. Control of phycoerythrin synthesis during chromatic adaptation. Plant Physiol. 64:786-90
52. Glazer AN. 1982. Phycobilisomes: structure and dynamics. Annu. Rev. Microbiol. 36:173-98
53. Grossman AR, Bhaya D, Apt KE, Kehoe DM. 1995. Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu. Rev. Genet. 29:231-88
54. Hattori A, Fujita Y. 1959. Effect of pre-illumination on the formation of phycobilin pigments in a blue-green alga, Tolypothrix tennis. J. Biochem. 46:1259-61
55. Hattori A, Fujita Y. 1959. Formation of phycobilin pigments in a blue-green alga, Tolypothrix tennis, as induced by illumination with colored lights. J. Biochem. 46:521-24
56. Haury JF, Bogorad L. 1977. Action spectra for phycobiliprotein synthesis in a chromatically adapting cyanophyte, Fremyella diplosiphon. Plant Physiol. 60:835-39
57. Herdman M, Castenholzh RW, Rippka R. 2001. Form genus III. Tolypothrix Kützing 1843. In Bergey's Manual of Systematic Bacteriology, ed. DR Boone, RW Castenholzh, pp. 587-89. New York: Springer
58. Houmard J, Capuano V, Colombano MV, Coursin T, Tandeau de Marsac N. 1990. Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes. Proc. Natl. Acad. Sci. USA 87:2152-56
59. Houmard J, Capuano V, Coursin T, Tandeau de Marsac N. 1988. Genes encoding core components of the phycobilisome in the cyanobacterium Calothrix sp. strain PCC 7601: occurrence of a multigene family. J. Bacteriol. 170:5512-21
60. Hughes J, Lamparter T. 1999. Prokaryotes and phytochrome. The connection to chromophores and signaling. Plant Physiol. 121:1059-68
61. Kahn K, Mazel D, Houmard J, Tandeau de Marsac N, Schaefer MR. 1997. A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. J. Bacteriol. 179:998-1006
62. Kehoe DM, Grossman AR. 1996. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409-12
63. Kehoe DM, Grossman AR. 1997. New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J. Bacteriol. 179:3914-21
64. Kehoe DM, Grossman AR. 1998. Use of molecular genetics to investigate complementary chromatic adaptation: advances in transformation and complementation. Meth. Enzymol. 297:279-90
65. Kendrick RE, Kronenberg GHM. 1994. Photomorphogenesis in Plants. Dordrecht: Kluwer-Martinus Nijhoff. 828 pp.
66. Lazaroff N, Schiff J. 1962. Action spectrum for developmental photo-induction of blue-green alga Nostoc muscorum. Science 137:603-4
67. Li L, Kehoe DM. 2005. In vivo analysis of the roles of conserved aspartate and histidine residues within a complex response regulator. Mol. Microbiol. 55:1538-52
68. Lomax TL, Conley PB, Schilling J, Grossman AR. 1987. Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA. J. Bacteriol. 169:2675-84
69. Luque I, Ochoa de Alda JAG, Richaud C, Zabulon G, Thomas JC, Houmard J. 2003. The NbIAI protein from the filamentous cyanobacterium Tolypothrix PCC 7601: regulation of its expression and interactions with phycobilisome components. Mol. Microbiol. 50:1043-54
70. MacColl R. 1998. Cyanobacterial phycobilisomes. J. Struct. Biol. 124:311-34
71. Mazel D, Guglielmi G, Houmard J, Sidler W, Bryant DA, Tandeau de Marsac N. 1986. Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7 601. Nucleic Acids Res. 14:8279-90
72. Mazel D, Houmard J, Castets AM, Tandeau de Marsac N. 1990. Highly repetitive DNA sequences in Cyanobacterial genomes. J. Bacteriol. 172:2755-61
73. Mazel D, Houmard J, 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
74. Mazel D, Marliere P. 1989. Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature 341:245-48
75. Montgomery BL, Casey ES, Grossman AR, Kehoe DM. 2004. AplA, a member of a new class of phycobiliproteins lacking a traditional role in photosynthetic light harvesting. J. Bacteriol. 186:7420-28
76. Montgomery BL, Lagarias JC. 2002. Phytochrome ancestry: sensors of bilins and light. Trends Plant. Sci. 7:357-66
77. Noubir S, Luque I, Ochoa de Alda JAG, Perewoska I, Tandeau de Marsac N, Cobley JG, Houmard J. 2002. Co-ordinated expression of phycobiliprotein operons in the chromatically adapting cyanobacterium Calothrix PCC 7601: a role for RcaD and RcaG. Mol. Microbiol. 43:749-62
78. Oelmüller R, Conley PB, Federspiel N, Briggs WR, Grossman AR. 1988. Changes in accumulation and synthesis of transcripts encoding phycobilisome components during acclimation of Fremyella diplosiphon to different light qualities. Plant Physiol. 88:1077-83
79. Oelmüller R, Grossman AR, Briggs WR. 1988. 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. 88:1084-91
80. Oelmüller R, Grossman AR, Briggs WR. 1989. Role of protein synthesis in regulation of phycobiliprotein mRNA abundance by light quality in Fremyella diplosiphon. Plant Physiol. 90:1486-91
81. Ohki K, Fujita Y. 1991. Complementary chromatic adaptation in the cyanobacterium, Tolypothrix tennis: location of phycoerythrin newly synthesized by green illumination. Plant Cell Physiol. 32:483-88
82. Ohki K, Fujita Y. 1992. Photoregulation of phycobilisome structure during complementary chromatic adaptation in the marine cyanophyte Phormidium sp. C86. J. Phycol. 28:803-8
83. Ohki K, Gantt E, Lipschultz CA, Ernst MC. 1985. Constant phycobilisome size in chromatically adapted cells of the cyanobacterium Tolypothrix tenuis, and variation in Nostoc sp. Plant Physiol. 79:943-48
84. Ohki K, Watanabe M, Fujita Y. 1982. Action of near UV and blue light on the photocontrol of phycobiliprotein formation; a complementary chromatic adaptation. Plant Cell Physiol. 23:651-56
85. Palenik B. 2001. Chromatic adaptation in marine Synechococcus strains. Appl. Environ. Microbiol. 67:991-94
86. Parkinson JS. 1995. Genetic approaches for signalling pathways and proteins. In Two-Component Signal Transduction, ed. JA Hoch, TJ Silhavy, pp. 9-23. Washington, DC: ASM Press
87. 2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance. FEMS Microbiol. Ecol. 37:117-25
88. Ramus J. 1983. A physiological test of the theory of complementary chromatic adaptation. II. Brown, green and red seaweeds. J. Phycol. 19:173-78
89. Ramus J, van der Meer JP. 1983. A physiological test of the theory of complementary chromatic adaptation. I. Color mutants of a red seaweed. J. Phycol. 19:86-91
90. Raven JA, Andrews M, Quigg A. 2005. The evolution of oligotrophy: implications for the breeding of crop plants for low input agricultural systems. Ann. Appl. Biol. 146:261-80
91. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111:1-61
92. Robinson BL, Miller JH. 1970. Photomorphogenesis in blue-green alga Nostoc commune 584. Physiol. Plant. 23:461-72
93. Rosinski J, Hainfeld JF, Rigbi M, Siegelman HW. 1981. Phycobilisome ultrastructure and chromatic adaptation in Fremyella diplosiphon. Ann. Bot. 47:1-12
94. Saffo MB. 1987. New light on seaweeds. Bioscience 37:654-64
95. Schmidt-Goff CM, Federspiel NA. 1993. In vivo and in vitro footprinting of a light-regulated promoter in the cyanobacterium Fremyella diplosiphon. J. Bacteriol. 175:1806-13
96. Seib LO, Kehoe DM. 2002. A turquoise mutant genetically separates expression of genes encoding phycoerythrin and its associated linker peptides. J. Bacteriol. 184:962-70
97. Sidler WA. 1994. Phycobilisome and phycobiliprotein structures. In The Molecular Biology of Cyanobacteria, ed. DA Bryant, pp. 139-216. Dordrecht: Kluwer Acad.
98. Siegelman HW, Hendricks SB. 1965. Purification and properties of phytochrome: a chromoprotein regulating plant growth. Fed. Proc. 24:863-67
99. Sobczyk A, Bely A, Tandeau de Marsac N, Houmard J. 1994. A phosphorylated DNA-binding protein is specific for the red-light signal during complementary chromatic adaptation in cyanobacteria. Mol. Microbiol. 13:875-85
100. Sobczyk A, Schyns G, Tandeau de Marsac N, 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
101. Stowe-Evans EL, Ford J, Kehoe DM. 2004. Genomic DNA microarray analysis: identification of new genes regulated by light color in the cyanobacterium Fremyella diplosiphon. J. Bacteriol. 186:4338-49
102. Stowe-Evans EL, Kehoe DM. 2004. Signal transduction during light-quality acclimation in cyanobacteria: a model system for understanding phytochrome-response pathways in prokaryotes. Photochem. Photobiol. Sci. 3:495-502
103. Tandeau de Marsac N. 1983. Phycobilisomes and complementary chromatic adaptation in cyanobacteria. Bull. Inst. Pasteur 81:201-54
104. Tandeau de Marsac N. 1977. Occurrence and nature of chromatic adaptation in cyanobacteria. J. Bacteriol. 130:82-91
105. Tandeau de Marsac N. 2003. Phycobiliproteins and phycobilisomes: the early observations. Photosynth. Res. 76:197-205
106. Tandeau de Marsac N, Castets AM, Cohen-Bazire G. 1980. Wavelength modulation of phycoerythrin synthesis in Synechocystis sp. 6701. J. Bacteriol. 142:310-14
107. Tandeau de Marsac N, Cohen-Bazire G. 1977. Molecular composition of cyanobacterial phycobilisomes. Proc. Natl. Acad. Sci. USA 74:1635-39
108. Tandeau de Marsac N, Mazel D, Damerval T, Guglielmi G, Capuano V, Houmard J. 1988. Photoregulation of gene expression in the filamentous cyanobacterium Calothrix sp. PCC 7601: light-harvesting complexes and cell differentiation. Photosynth. Res. 18:99-132
109. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506
110. Terauchi K, Montgomery BL, Grossman AR, Lagarias JC, Kehoe DM. 2004. RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol. Microbiol. 51:567-77
111. Vierstra RD. 2003. Cyanophytochromes, bacteriophytochromes, and plant phytochromes: light-regulated kinases related to bacterial two-component regulators. In Histidine Kinases in Signal Transduction, ed. M Inouye, R Dutta, pp. 273-95. San Diego, CA: Academic
112. Vogelmann TC, Scheibe J. 1978. Action spectra for chromatic adaptation in the blue-green alga Fremyella diplosiphon. Planta 143:233-39
113. Westermann M, Wehrmeyer W. 1995. A new type of complementary chromatic adaptation exemplified by Phormidium sp. C86: changes in the number of peripheral rods and in the stoichiometry of core complexes in phycobilisomes. Arch. Microbiol. 164:132-41