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Phycobilisome structure and function

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Abstract

Phycobilisomes are aggregates of light-harvesting proteins attached to the stroma side of the thylakoid membranes of the cyanobacteria (blue-green algae) and red algae. The water-soluble phycobiliproteins, of which there are three major groups, tetrapyrrole chromophores covalently bound to apoprotein. Several additional protiens are found within the phycobilisome and serve to link the phycobiliproteins to each other in an ordered fashion and also to attach the phycobilisome to the thylakoid membrane. Excitation energy absorbed by phycoerythrin is transferred through phycocyanin to allophycocyanin with an efficiency approximating 100%. This pathway of excitation energy transfer, directly confirmed by time-resolved spectroscopic measurements, has been incorporated into models describing the ultrastructure of the phycobilisome. The model for the most typical type of phycobilisome describes an allophycocyanin-containing core composed of three cylinders arranged so that their longitudinal axes are parallel and their ends form a triangle. Attached to this core are six rod structures which contain phycocyanin proximal to the core and phycoerythrin distal to the core. The axes of these rods are perpendicular to the longitudinal axis of the core. This arrangement ensures a very efficient transfer of energy. The association of phycoerythrin and phycocyanin within the rods and the attachment of the rods to the core and the core to the thylakoid require the presence of several ‘linker’ polypeptides. It is recently possible to assemble functionally and structurally intact phycobilisomes in vitro from separated components as well as to reassociate phycobilisomes with stripped thylakoids. Understanding of the biosynthesis and in vivo assembly of phycobilisomes will be greatly aided by the current advances in molecular genetics, as exemplified by recent identification of several genes encoding phycobilisome components.

Combined ultrastructural, biochemical and biophysical approaches to the study of cyanobacterial and red algal cells and isolated phycobilisome-thylakoid fractions are leading to a clearer understanding of the phycobilisome-thylakoid structural interactions, energy transfer to the reaction centers and regulation of excitation energy distribution. However, compared to our current knowledge concerning the structural and functional organization of the isolated phycobilisome, this research area is relatively unexplored.

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References

  1. Anderson LK, Rayner MC, Sweet RM and Eiserling FA (1983) Regulation of Nostoc sp. phycobilisome structure by light and temperature. J Bact 155:1407–1416.

    Google Scholar 

  2. Belford HS, Offner GD and Troxler RF (1983) Phycobiliprotein synthesis in the unicellular rhodophyte, Cyanidium caldarium: cell-free translation of the mRNAS for the α and β subunit polypeptides of phycocyanin. J Biol Chem 258:4503–4510.

    Google Scholar 

  3. Bennett A and Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435.

    Google Scholar 

  4. Berns DS (1967) Immunochemistry of biliproteins. Plant Physiol 42:1569–1586.

    Google Scholar 

  5. Biggins J (1983) Mechanism of the light state transition in photosynthesis. I. Analysis of the kinetics of cytochrome oxidation in state 1 and state 2 in the red alga, Porphyridium cruentum. Biochim Biophys Acta 724:111–117.

    Google Scholar 

  6. Biggins J and Bruce D (1985) Mechanism of the light state transition in photosynthesis. III. Kinetics of the state transition in Porphyridium cruentum. Biochim Biophys Acta 806:230–236.

    Google Scholar 

  7. Biggins J, Campbell CL and Bruce D (1984) Mechanism of the light state transition in photosynthesis II. Analysis of phosphorylated polypeptides in the red alga, Porphyridium cruentum. Biochim Biophys Acta 767:138–144.

    Google Scholar 

  8. Bogorad L (1975) Phycobiliproteins and complementary chromatic adaptation. Ann Rev Plant Physiol 26:369–401.

    Google Scholar 

  9. Brody SS, Porter G, Tredwell CJ and Barber J (1981) Picosecond energy transfer in Anacystis nidulans. Photobiochem Photobiophys 2:11–14.

    Google Scholar 

  10. Brody SS, Tredwell C and Barber J (1981) Picosecond energy transfer in Porphyridium cruentum and Anacystis nidulans. Biophys J 34:439–449.

    Google Scholar 

  11. Brown AS, Offner GD, Enrhardt MM and Troxler RF (1979) Phycobilin-apoprotein linkages in the α and β subunits from the unicellular rhodophyte, Cyanidium caldarium. Amino acid sequences of 35S-labelled chromopeptides. J Biol Chem 254:7803–7811.

    Google Scholar 

  12. Bruce D, Biggins J, Steiner T and Thelwalt M (1985) Mechanism of the light state transition in photosynthesis. IV. Picosecond fluorescence spectroscopy of Anacystis nidulans and Porphyridium cruentum in state 1 and state 2 at 77 K. Biochim Biophys Acta 806:237–246.

    Google Scholar 

  13. Bryant DA (1981) The photoregulated expression of multiple phycocyanin species. A general mechanism for the control of phycocyanin synthesis in chromatically adapting cyanobacteria. Eur J Biochem 119:425–429.

    Google Scholar 

  14. Bryant DA (1982) Phycoerythrocyanin and phycoerythrin: properties and occurrence in cyanobacteria. J Gen Microbiol 128:835–844.

    Google Scholar 

  15. 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.

    Google Scholar 

  16. Bryrant DA, Guglielmi G, Tandeau de Marsac N, Castets AM and Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisomes: A model. Arch Microbiol 123:113–127.

    Google Scholar 

  17. Bryant DA, de Lorimer R, Lambert DH, Dubbs JM, Stirewalt VL, Stevens SE, Porter RD, Tam J and Jay E (1985) Molecular cloning and nucleotide sequence of the α and β subunits of allophycocyanin from the cyanelle genome of Cyanophora paradoxa. Proc Natl Acad Sci USA 82:3242–3246.

    Google Scholar 

  18. Canaani O and Gantt E (1982) Formation of hybrid phycobilisomes by association of phycobiliproteins from Nostoc and Fremyella. Proc Natl Acad Sci USA 79: 5277–5281.

    Google Scholar 

  19. Clement-Metral JD, Gantt E and Redlinger T (1983) A photosystem II-phycobilisome preparation from the red alga, Porphyridium cruentum: oxygen evolution, ultrastructure, and polypeptide resolution. Arch Biochem Biophys 238:10–17.

    Google Scholar 

  20. Cohen-Bazire G, Beguin S, Rimon S, Glazer AN and Brown DM (1977) Physiochemical and immunological properties of allophycocyanins. Arch Microbiol 111:225–238.

    Google Scholar 

  21. Cohen-Bazire G and Bryant DA (1982) Phycobilisomes: Composition and structure. In Carr NG and Whitton BA (eds). The Biology of Cyanobacteria, pp 43–190. Oxford: Blackwell Sci Publ.

    Google Scholar 

  22. Csatorday K, MacColl R, Csizmadia V, Grabowski J and Bagyinka C (1984) Exciton interaction in allophycocyanin. Biochemistry 23:6466–6470.

    Google Scholar 

  23. Dagen AJ, Alfano RR, Zilinskas BA and Swenberg CE (1985) Fluorescence kinetics of emission from a small finite volume of a biological system. Chem Physics 96:483–488.

    Google Scholar 

  24. Dagen AJ, Alfano RR, Zilinskas BA and Swenberg CE (1986) Analysis of fluorescence kinetics and energy transfer in the isolated α subunit of phycoerythrin from Nostoc sp. Photochem Photobiol 43:71–79.

    Google Scholar 

  25. Dale RE and Teale FWJ (1970) Number and distribution of chromophore types in native phycobiliproteins. Photochem Photobiol 12:99–117.

    Google Scholar 

  26. Dilworth MF and Gantt E (1981) Phycobilisome-thylakoid topography of photosynthetically active vesicles of Porphyridium cruentum. Plant Physiol 67:608–612.

    Google Scholar 

  27. Diner BA (1979) Energy transfer from phycobilisomes to photosystem II reaction centers in wild type Cyanidium caldarium. Plant Physiol 63:30–34.

    Google Scholar 

  28. Doukas AG, Stefanic V, Buchert J, Alfano RR and Zilinskas BA (1981) Exciton annihilation in the isolated phycobiliproteins from the blue-green alga Nostoc sp. using picosecond absorption spectroscopy. Photochem Photobiol 34:505–510.

    Google Scholar 

  29. Duysens LNM, Amesz J and Kamp BM (1961) Two photochemical systems in photosynthesis. Nature 190:510–511.

    Google Scholar 

  30. Egelhoff T and Grossman A (1983) Cytoplasmic and chloroplast synthesis of phycobilisome polypeptides. Proc Natl Acad Sci USA 80:3339–3343.

    Google Scholar 

  31. Fork DC and Satoh K (1983) State I-State II transitions in the thermophilic blue-green alga (cyanobacterium) Synechococcus lividus. Photochem Photobiol 37:421–427.

    Google Scholar 

  32. Frank G, Sidler W, Widmer H and Zuber H (1978) Complete amino acid sequences of both subunits of C-phycocyanin from the cyanobacterium Mastigocladus laminosus. Hoppe-Seyler's Z Physiol Chem 359:1491–1507.

    Google Scholar 

  33. Fuglistaller P, Suter F and Zuber H (1983) The complete amino-acid sequence of both subunits of phycoerythrocyanin from the thermophilic cyanobacterium Mastigocladus laminosus. Hoppe-Seyler's Z Physiol Chem 364:691–712.

    Google Scholar 

  34. Fuglistaller P, Rumbeli R, Suter F and Zuber H (1984) Minor polypeptides from the phycobilisomes of the cyanobacterium, Mastigocladus laminosus. Isolation, characterization and amino acid sequences of a colorless 8.9 kD polypeptide and of a 16.2 kD phycobiliprotein. Hoppe-Seyler's Z Physiol Chem 365:1085–1096.

    Google Scholar 

  35. Gantt E (1975) Phycobilisomes: Light-harvesting pigment complexes. Bioscience 25:781–788.

    Google Scholar 

  36. Gantt E (1980) Structure and function of phycobilisomes: light harvesting pigment complexes in red and blue-green algae. Int Rev Cytol 66:45–80.

    Google Scholar 

  37. Gantt E (1981) Phycobilisomes. Ann Rev Plant Physiol 32:327–347.

    Google Scholar 

  38. Gantt E and Conti SF (1966) Phycobiliprotein localization in algae. Brookhaven Symp Biol 19:393–405.

    Google Scholar 

  39. Gantt E and Conti SF (1966) Granules associated with the chloroplast lamellae of Porphyridium cruentum. J Cell Biol 29:423–434.

    Google Scholar 

  40. Gantt E and Lipschultz CA (1972) Phycobilisomes of Porphyridium cruentum. I. Isolation. J Cell Biol 54:313–324.

    Google Scholar 

  41. Gantt E, Lipschultz CA, Grabowski J and Zimmerman BK (1979) Phycobilisomes from blue-green and red algae: isolation criteria and dissociation characteristics. Plant Physiol 63:615–620.

    Google Scholar 

  42. Gantt E, Lipschultz CA and Zilinsaks BA (1976) Further evidence for a phycobilisome model from selective dissociation, fluorescence emission, immunoprecipitation and electron microscopy. Biochim Biophys Acta 430:375–388.

    Google Scholar 

  43. Gendel S, Ohad I and Bogorad L (1979) Control of phycoerythrin synthesis during chromatic adaptation. Plant Physiol 64:786–790.

    Google Scholar 

  44. Giddings T and Staehelin LA (1979) Changes in thylakoid structure associated with differentiation of heterocysts in the cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 546:373–382.

    Google Scholar 

  45. Giddings TH, Wassman C and Staehelin LA (1983) Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiol 71:409–419.

    Google Scholar 

  46. Gillbro T, Sandstrom A, Sundstrom V and Holzwarth AR (1983) Polarized absorption picosecond kinetics as a probe of energy transfer in phycobilisomes of Synechococcus 6301 FEBS Lett 162:64–68.

    Google Scholar 

  47. Gingrich JC, Blaha LK and Glazer AN (1982) Rod substructure in cyanobacterial phycobilisomes: Analysis of Synechocystis 6701 mutants low in phycoerythrin. J Cell Biol 92:261–268.

    Google Scholar 

  48. Gingrich JC, Lundell DJ and Glazer AN (1983) Core substructure in cyanobacterial phycobilisomes. J Cell Biochem 22:1–14.

    Google Scholar 

  49. Gingrich JC, Williams RC and Glazer AN (1982) Rod substructure in cyanobacterial phycobilisomes: phycoerythrin assembly in Synechocystis 6701 phycobilisomes. J Cell Biol 95:170–178.

    Google Scholar 

  50. Glazer AN (1980) Structure and evolution of photosynthetic accessory pigment systems with special reference to phycobiliproteins. In Sigman DS and Brazier MAB, eds. The Evolution of Protein Structure and Function, pp. 221–244. New York: Academic Press.

    Google Scholar 

  51. Glazer AN (1982) Phycobilisomes: structure and dynamics. Ann Rev Microbiol 36:173–198.

    Google Scholar 

  52. Glazer AN (1983) Comparative biochemistry of photosynthetic light-harvesting systems. Ann Rev Biochem 52:125–157.

    Google Scholar 

  53. Glazer AN (1984) Phycobilisomes: a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768:29–51.

    Google Scholar 

  54. Glazer AN (1985) Light harvesting in phycobilisomes. Ann Rev Biophys and Biophys Chem 14:47–77.

    Google Scholar 

  55. Glazer AN and Bryant DA (1975) Allophycocyanin B (λmax 671,618nm). A new cyanobacterial phycobiliprotein. Arch Microbiol 104:15–22.

    Google Scholar 

  56. Glazer AN, Cohen-Bazire G and Stanier RY (1971) Comparative immunology of algal biliproteins. Proc Natl Acad Sci USA 42:3005–3008.

    Google Scholar 

  57. Glazer AN, Williams RC, Yamanaka G and Schachman HK (1979) Characterization of cyanobacterial phycobilisomes in zwitterionic detergents. Proc Natl Sci USA 76:6162–6166.

    Google Scholar 

  58. Glazer AN, Yeh SW, Webb SP and Clark JH (1985) Disk-to-disk transfer as the rate-limiting step for energy flow in phycobilisomes. Science 227:419–423.

    Google Scholar 

  59. Glick RE, Triemer RE and Zilinskas BA (1985) Freeze-fracture analysis of thylakoid membranes and photosystem I and II enriched fractions from Phormidium laminosum. J Cell Science, in press.

  60. Glick RE and Zilkinskas BA (1983) Role of the colorless polypeptides in phycobilisome reconstitution from separated phycobiliproteins. Plant Physiol 69:991–997.

    Google Scholar 

  61. Govindjee, Amesz J and Fork DC (1986) Light emission by plants and bacteria. Orlando: Academic Press.

    Google Scholar 

  62. Grabowski J and Gantt E (1978) Photophysical properties of phycobilisomes: fluorescence lifetimes, quantum yields and polarization spectra. Photochem Photobiol 28:39–45.

    Google Scholar 

  63. Guard-Friar D, MacColl R, Berns DS, Wittmershaus B and Knox RS (1985) Picosecond fluorescence of cryptomonad biliproteins. Effects of excitation intensity and the fluorescence decay times of phycocyanin 612, phycocyanin 645, and phycoerythrin 545. Biophys J 47:787–793.

    Google Scholar 

  64. Hanzlik CA, Hacock LE, Knox RS, Guard-Friar D and MacColl R (1985) Picosecond fluorescence spectroscopy of the biliprotein phycocyanin 612: direct evidence for fast energy transfer. J Luminescence 34:99–106.

    Google Scholar 

  65. Haworth P and Melis A (1983) Phosphorylation of chloroplast thylakoid membrane proteins does not increase the absorption cross-section of photosystem I. FEBS 160:277–280.

    Google Scholar 

  66. Hefferle P, John W, Scheer H and Schneider S (1984) Thermal denaturation of monomeric and trimeric phycocyanins studied by static and polarized time-resolved fluorescence spectroscopy. Photochem Photobiol 39:221–232.

    Google Scholar 

  67. Hefferle P, Nies M, Wehrmeyer W and Schneider S (1983) Picosecond time-resolved fluorescence study of the antenna system isolated from Mastigocladus laminosus Cohn. I. Functionally intact phycobilisomes. Photobiochem Photobiophys 5:41–51.

    Google Scholar 

  68. Hefferle P, Nies M, Wehrmeyer W and Schneider S (1983) Picosecond time-resolved fluorescence study of the antenna system isolated from Mastigocladus laminosus Cohn. II. Constituent biliproteins in various forms of aggregation. Photobiochem Photobiophys 5:325–334.

    Google Scholar 

  69. Hiller RG, Post A and Stewart AC (1983) Isolation of intact detergent-free phycobilisomes by trypsin. FEBS Lett 156:180–184.

    Google Scholar 

  70. Holzworth AR, Wendler J and Wehrmeyer W (1982) Picosecond time-resolved energy transfer in isolated phycobilisomes from Rhodella violacea. Photochem Photobiol 36:479–487.

    Google Scholar 

  71. Holzworth AR, Wendler J and Wehrmeyer W (1983) Studies on chromophore coupling in isolated phycobiliproteins. I. Picosecond fluorescence kinetics of energy transfer in phycocyanin from Chroomonas sp.. Biochim Biophys Acta 724: 388–395.

    Google Scholar 

  72. Karukstis KK and Sauer K (1984) Energy transfer and distribution in the red alga Porphyra perforata studied using picosecond fluorescence spectroscopy. Biochim Biophys Acta 766:141–147.

    Google Scholar 

  73. Katoh T and Gantt E (1979) Photosynthetic vesicles with bound phycobilisomes from Anabaena variabilis. Biochim Biophys Acta 546:383–393.

    Google Scholar 

  74. Kawamura M, Mimuro M and Fujita Y (1979) Quantitative relationship between two reaction centers in the photosynthetic system of blue-green algae. Plant Cell Physiol 20:697–705.

    Google Scholar 

  75. Khanna R, Graham J-R, Myers J and Gantt E (1983) Phycobilisome composition and possible relationship to reaction centers. Arch Biochem Biophys 224:534–542.

    Google Scholar 

  76. Kipe-Nolt JA, Stevens SE and Bryant DA (1982) Growth and chromatic adaptation of Nostoc sp. strain MAC and the pigment mutant R-MAC. Plant Physiol 70:1549–1553.

    Google Scholar 

  77. Kirilovsky D, Kessel M and Ohad I (1983) In vitro reassociation of phycobiliproteins and membranes to form functional membrane-bound phycobilisomes. Biochim Biophys Acta 724:416–426.

    Google Scholar 

  78. Kirilovsky D, Lavintman N, Ish-Shalom D and Ohad I (1984) Specificity of energy transfer to photosystem II by in vitro reassociated homologous and heterologous membrane-bound phycobilisomes. Biochim Biophys Acta 767:451–459.

    Google Scholar 

  79. Klotz AV and Glazer AN (1985) Characterization of the bilin attachment sites in R-phycoerythrin. J Biol Chem 260:4856–4863.

    Google Scholar 

  80. Kobayashi T, Degenkolb ED, Bersohn R, Rentzepis PM, MacColl R and Berns DS (1979) Energy transfer among the chromophores in phycocyanins measured by picosecond kinetics. Biochemistry 18:5073–5078.

    Google Scholar 

  81. Koller KP, Wehrmeyer W and Morschel E (1978) Biliprotein assembly in the discshaped phycobilisomes of Rhodella violacea. Eur J Biochem 91:57–63.

    Google Scholar 

  82. Kursar TA and Alberte RS (1983) Photosynthetic unit organization in a red alga. Relationships between light harvesting pigments and reaction centers. Plant Physiol 72:409–414.

    Google Scholar 

  83. Kursar TA, van der Meer J and Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigment mutations. Plant Physiol 73:353–360.

    Google Scholar 

  84. Kursar TA, van der Meer J and Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. II. Phycobilisome characteristics of pigment mutants. Plant Physiol 73: 361–369.

    Google Scholar 

  85. Kyle DJ, Staehlein CA and Arntzen CJ (1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222:527–541.

    Google Scholar 

  86. Lefort-Tran M, Cohen-Bazire G and Pouphile M (1973) Les membranes photosynthetiques des algues a biliproteins observee apres cryodecapage. J Ultrastr Res 44: 3957–3960.

    Google Scholar 

  87. Lemaux PG and Grossman A (1984) Isolation and characterization of a gene for a major light-harvesting polypeptide from Cyanophora paradoxa. Proc Natl Acad USA 81:4100–4104.

    Google Scholar 

  88. Lemaux PG and Grossman AR (1985) Major light harvesting polypeptides in polycistronic transcripts in a eukaryotic alga. EMBO J 4: 1911–1919.

    Google Scholar 

  89. Ley AC (1984) Effective absorption cross-sections in Porphyridium cruentum. Implications for energy transfer between phycobilisomes and photosystem II reaction centers. Plant Physiol 74:451–454.

    Google Scholar 

  90. Ley AC and Butler WL (1980) Energy distribution in the photochemical apparatus of Porphyridium cruentum in State I and State II. Biochim Biophys Acta 592:349–363.

    Google Scholar 

  91. Ley AC and Butler WL (1980) Effects of chromatic adaptation on the photochemical apparatus of photosynthesis in Porphyridium cruentum. Plant Physiol 65:714–722.

    Google Scholar 

  92. Ley AC, Butler WL, Bryant DA and Glazer AN (1977) Isolation and function of allophycocyanin B of Porphyridium cruentum. Plant Physiol 59:974–980.

    Google Scholar 

  93. Lichtle C and Thomas JC (1976) Etude ultrastructurale des thylacoides des algues a phycobiliproteines, comparason des resultats obtenus par fixation classiquel et cryodecapage. Phycologia 15:393–404.

    Google Scholar 

  94. de Lorimer R, Bryant DA, Porter RD, Liu W-Y, Jay E and Stevens SE (1984) Genes for the α and β subunits of phycocyanin. Proc Natl Acad Sci USA 81:7946–7950.

    Google Scholar 

  95. Lundell DJ and Glazer AN (1981) Allophycocyanin B: a common subunit in Synechococcus allophycocyanin B (λmax 670 nm) and allophycocyanin (λmax 650 nm). J Biol Chem 256:12600–12606.

    Google Scholar 

  96. Lundell DJ and Glazer AN (1983) Molecular architecture of a light-harvesting antenna: structure of the 18S core-rod subassembly of the Synechococcus 6301 phycobilisome. J Biol Chem 258: 894–901.

    Google Scholar 

  97. Lundell DJ and Glazer AN (1983) Molecular architecture of a light-harvesting antenna: core substructure in Synechococcus 6301 phycobilisomes: two new allophycocyanin and allophycocyanin B complexes. J Biol Chem 258: 902–908.

    Google Scholar 

  98. Lundell DJ and Glazer AN (1983) Molecular architecture of a light-harvesting antenna: quarternary interactions in the Synechococcus 6301 phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies. J Biol Chem 258:8708–8713.

    Google Scholar 

  99. Lundell DJ, Williams RC and Glazer AN (1981) Molecular architecture of a light-harvesting antenna: in vitro assembly of the rod substructures of Synechococcus 6301 phycobilisomes. J Biol Chem 256:3580–3592.

    Google Scholar 

  100. Lundell DJ, Yamanaka G and Glazer AN (1981) A terminal energy acceptor of the phycobilisomes: the 75,000 dalton polypeptide of Synechococcus 6301 phycobilisomes — a new biliprotein. J Cell Biol 91:315–319.

    Google Scholar 

  101. MacColl R (1982) Phycobilisomes and biliproteins. Photochem Photobiol 35: 899–904.

    Google Scholar 

  102. MacColl R and Berns DS (1981) Biliproteins: some relationships among aggregation states, spectra and excitation energy transfer. Israel J Chem 21:296–300.

    Google Scholar 

  103. MacColl R, Csatorday K, Berns DS and Traeger E (1981) The relationship of the quarternary structure of allophycocyanin to its spectrum. Arch Biochem Biophys 208:42–48.

    Google Scholar 

  104. Manodori A, Alhadeff M, Glazer AN and Melis A (1984) Photochemical apparatus organization in Synechococcus 6301 (Anacystis nidulans). Effect of phycobilisome mutation. Arch Microbiol 139:117–123.

    Google Scholar 

  105. Manodori A and Melis A (1984) Photochemical apparatus organization in Anacystis nidulans (Cyanophyceae). Effect of CO2 concentration during cell growth. Plant Physiol 74:67–71.

    Google Scholar 

  106. Manodori A and Melis A (1985) Phycobilisome-photosystem II association in Synechococcus 6301 (Cyanophyceae). FEBS Lett 181:79–82.

    Google Scholar 

  107. Mimuro M, Yamazaki I, Murao T, Yamazaki T, Yoshihara K and Fujita T (1984) Excitation energy transfer in phycobilin-chlorophyll a system in blue-green and red algae. In Sybesma C, ed. Advances in Photosynthesis Research I, pp. 21–28. The Hague/Junk.

    Google Scholar 

  108. Mimuro M, Yamazaki I, Yamazaki T and Fujita Y (1985) Excitation energy transfer in the chromatically adapted phycobilin systems of blue-green algae: difference in the energy transfer kinetics at phycocyanin level. Photochem Photobiol 41: 597–603.

    Google Scholar 

  109. Morschel E, Koller KP, Wehrmeyer W and Schneider H (1977) Biliprotein assembly in the disc-shaped phycobilisomes of Rhodella violacea. I. Electron microscopy of phycobilisomes in situ and analysis of their architecture after isolation and negative staining. Cytobiologie 16:118–129.

    Google Scholar 

  110. Murata N (1969) Control of excitation energy transfer in photosynthesis. I. Light-induced change of chl a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251.

    Google Scholar 

  111. Myers J, Graham JR and Wang RTK (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149.

    Google Scholar 

  112. Neushul M (1970) A freeze-etching study of the red alga Porphyridium. Am J Bot 57:1231–1239.

    Google Scholar 

  113. Nies M and Wehrmeyer W (1981) Biliprotein assembly in the hemidiscoidal phycobilisomes of the thermophilic cyanobacterium Mastigocladus laminosus Cohn. Characterization of dissociation products with special reference to the peripheral phycoerythrocyanin-phycocyanin complexes. Arch Microbiol 129:374–379.

    Google Scholar 

  114. Offner GD and Troxler RF (1983) Primary structure of allophycocyanin from the unicellular rhodophyte, Cyandium caldarium. J Biol Chem 258:9931–9940.

    Google Scholar 

  115. Pakrashi HB and Sherman LA (1984) A highly active oxygen-evolving photosystem II preparation from the cyanobacterium Anacystis nidulans. Plant Physiol 74:742–745.

    Google Scholar 

  116. Pellegrino F, Wong D, Alfano RR and Zilinskas BA (1981) Fluorescence relaxation kinetics and quantum yields from the phycobilisomes of the blue-green alga Nostoc sp. measured as a function of single picosecond pulse intensity. Photochem Photobiol 34:691–696.

    Google Scholar 

  117. Pilot TJ and Fox JL (1984) Cloning and sequencing of the genes encoding the α and β subunits of C-phycocyanin from the cyanobacterium Agmenellum quadruplicatum. Proc Natl Acad Sci USA 81:6983–6987.

    Google Scholar 

  118. 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.

    Google Scholar 

  119. Rapoport H and Glazer AN (1985) Bilins and bilin-protein linkages in phycobiliproteins: structural and spectroscopic studies. In Blauer G and Sund H, eds, Optical Properties and Structure of Tetrapyrroles. pp. 411–427. New York: Walter de Gruyter and Co.

    Google Scholar 

  120. Redlinger T and Gantt E (1981) Phycobilisome structure of Porphyridium cruentum. Polypeptide composition. Plant Physiol 68:1375–1379.

    Google Scholar 

  121. Redlinger T and Gantt E (1982) A Mr 95 000 polypeptide in Porphyridium cruentum phycobilisomes and thylakoids: possible function in linkage of phycobilisomes to thylakoids and in energy transfer. Proc Natl Acad Sci USA 79:5542–5546.

    Google Scholar 

  122. Ried A and Reinhardt B (1980) Distribution of excitation energy between photosystem I and photosystem II in red algae. Biochim Biophys Acta 592:76–86.

    Google Scholar 

  123. Rigbi M, Rosinski J, Siegelman HW and Sutherland JC (1980) Cyanobacterial phycobilisomes: Selective dissociation monitored by fluorescence and circular dichroism. Proc Natl Acad Sci USA 77:1961–1965.

    Google Scholar 

  124. Rusckowski M and Zilinskas BA (1980) Chlorophyll-protein complexes of the cyanophyte Nostoc sp. Plant Physiol 65:392–396.

    Google Scholar 

  125. Rusckowski M and Zilinskas BA (1982) Allophycocyanin I and the 95 kilodalton polypeptide. The bridge between phycobilisomes and membranes. Plant Physiol 70:1055–1059.

    Google Scholar 

  126. Satoh K and Fork DC (1983) A new mechanism for adaptation to changes in light intensity and quality in the red alga, Porphyra perforata I. Relation to state 1 and state 2 transitions. Biochim Biophys Acta 722:109–196.

    Google Scholar 

  127. Scheer H (1981) Biliproteins. Angew Chem Int Ed Engl 20:241–261.

    Google Scholar 

  128. Scheer H (1982) Phycobiliproteins: molecular aspects of photosynthetic antenna system. In Fong FK, ed. Molecular Biology, Biochemistry and Biophysics. Vol. 35. Light Reaction Path of Photosynthesis, pp. 7–45. New York: Springer-Verlag.

    Google Scholar 

  129. Schirmer T, Bode W, Huber R, Sidler W and Zuber H (1985) X-ray crystallographic structure of the light-harvesting biliprotein c-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. J Mol Biol 184:257–277.

    Google Scholar 

  130. Schuster G, Owens GC, Cohen Y and Ohad I (1984) Thylakoid polypeptide composition and light-dependent phosphorylation of the chlorophyll a/b-protein in Prochloron, a prokaryote exhibiting oxygen evolving photosynthesis. Biochim Biophys Acta 767:596–605.

    Google Scholar 

  131. 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.

    Google Scholar 

  132. Sidler W, Gysi J, Isker E and Zuber H (1981) The complete amino acid sequence of both subunits of allophycocyanin, a light harvesting protein-pigment complex from the cyanobacterium Mastigocladus laminosus. Hoppe-Seyler's Z Physiol Chem 362:611–628.

    Google Scholar 

  133. Siegelman HW and Kycia JH (1982) Molecular morphology of cyanobacterial phycobilisomes. Plant Physiol 70:887–897.

    Google Scholar 

  134. Staehelin CA and Arntzen CJ (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J Cell Biol 92:1327–1337.

    Google Scholar 

  135. Staehelin LA, Giddings TH, Badami P and Krzymowski WW (1978) A comparison of the supramolecular architecture of photosynthetic membranes of blue-green, red, and green algae and of higher plants. In Deamer D, ed. Light Transducing Membranes pp. 335–355. New York: Academic Press.

    Google Scholar 

  136. Stevens CLR and Myers J (1976) Characterization of pigment mutants in a blue-green alga, Anacystis nidulans. J Phycol 12:99–105.

    Google Scholar 

  137. Suter GW, Mazzola P, Wendler J and Holzwarth AR (1984) Fluorescence decay kinetics in phycobilisomes isolated from the blue-green alga Synechococcus 6301. Biochim Biophys Acta 766:269–276.

    Google Scholar 

  138. Switalski SC and Sauer K (1984) Energy transfer among the chromophores of c-phycocyanin from Anabaena variabilis using steady state and time-resolved fluorescence spectroscopy. Photochem Photobiol 40:423–427.

    Google Scholar 

  139. Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130:82–91.

    Google Scholar 

  140. Tandeau de Marsac N (1983) Phycobilisomes and complementary chromatic adaptation in cyanobacteria. Bull de L'Inst Pasteur 81:201–254.

    Google Scholar 

  141. Tandeau de Marsac N and Cohen-Bazire G (1977) Molecular composition of cyanobacterial phycobilisomes. Proc Natl Acad Sci USA 74:1635–1639.

    Google Scholar 

  142. Tredwell CJ, Synowiec JA, Searle GFW, Porter G and Barber J (1978) Picosecond time-resolved fluorescence of chlorophyll in vivo. Photochem Photobiol 28:1013–1020.

    Google Scholar 

  143. Troxler RF and Brown A (1970) Biosynthesis of phycocyanin in vivo. Biochim Biophys Acta 215:503–511.

    Google Scholar 

  144. Troxler RF, Foster JA, Brown AS and Franzblau C (1975) The α and β subunits of Cyanidium caldarium phycocyanin: properties and amino acid sequences at the amino terminus. Biochemistry 14:268–274.

    Google Scholar 

  145. Waaland JR, Waaland SD and Bates G (1974) Chloroplast structure and pigment composition in the red alga Griffithsia pacifica: regulation by light intensity. J Phycol 10:193–199.

    Google Scholar 

  146. Wehrmeyer W (1983) Phycobiliproteins and phycobiliprotein organization in the photosynthetic apparatus of cyanobacteria, red algae, and cryptophytes. In Jensen U and Fairbrothers DE eds. Proteins and Nucleic Acids in Plant Systematics, pp. 143–167. New York:Springer Verlag.

    Google Scholar 

  147. Wehrmeyer W, Wendler J and Holzwarth AR (1985) Biochemical and functional characterization of a peripheral phycobilisome unit from Porphyridium cruentum. Measurement of picosecond energy transfer kinetics. Eur J Cell Biol 36:17–23.

    Google Scholar 

  148. Wendler J, Holzwarth AR and Wehrmeyer W (1984) Picosecond time-resolved energy transfer in phycobilisomes isolated from the red alga Porphyridium cruentum. Biochim Biophys Acta 765:58–67.

    Google Scholar 

  149. Williams RC, Gingrich JC and Glazer AN (1980) Cyanobacterial phycobilisomes: particles from Synechocystis 6701 and two pigment mutants. J Cell Biol 85:558–566.

    Google Scholar 

  150. Wollman FA (1979) Ultrastructural comparison of Cyanidium caldarium wild type and III-C mutant lacking phyobilisomes. Plant Physiol 63:375–381.

    Google Scholar 

  151. Wong D, Pellergrino F, Alfano RR and Zilinskas BA (1981) Fluorescence relaxation kinetics and quantum yield from the isolated phycobiliproteins of single picosecond pulse intensity. Photochem Photobiol 33:651–662.

    Google Scholar 

  152. Yamagishi A and Katoh S (1984) A photoactive photosystem II reaction center complex lacking a chlorophyll-binding 40 kilodalton subunit from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 765:118–124.

    Google Scholar 

  153. Yamanaka G, Glazer AN and Williams RC (1978) Cyanobacterial phycobiblisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301. J Biol Chem 253:8303–8310.

    Google Scholar 

  154. Yamanaka G, Glazer AN and Williams RC (1980) Molecular architecture of a light-harvesting antenna. Comparison of wild type and mutant Synechococcus 6301 phycobilisomes. J Biol Chem 255:11004–11010.

    Google Scholar 

  155. Yamanaka G, Lundell DJ and Glazer AN (1982) Molecular architecture of a light-harvesting antenna. Isolation and characterization of phycobilisome subassembly particles. J Biol Chem 257:4077–4086.

    Google Scholar 

  156. Yamazaki I, Mimuro M, Murao T, Yamazaki T, Yoshihara K and Fujita Y (1984) Excitation energy transfer in the light-harvesting antenna system of the red alga Porphyridium cruentum and the blue-green alga Anacystis nidulans: analysis of time-resolved fluorescence spectra. Photochem Photobiol 39:233–240.

    Google Scholar 

  157. Yu M and Glazer AN (1982) Cyanobacterial phycobilisomes. Role of the linker polypeptides in the assembly of phycocyanin. J Biol Chem 257:3429–3433.

    Google Scholar 

  158. Yu M, Glazer AN and Williams RC (1981) Cyanobacterial phycobilisomes. Phycyanin assembly in the rod substructures of Anabaena variabilis phycobilisomes. J Biol Chem 256:13130–13136.

    Google Scholar 

  159. Zilinskas BA (1981) Phycobiliprotein complexes of the cyanophyte, Nostoc sp. In Akoyunoglu G, ed. Photosynthesis III. Structure and Molecular Organization of the Photosynthetic Apparatus, pp. 365–375. Philadelphia: Balaban International Science Service.

    Google Scholar 

  160. Zilinskas BA (1982) Isolation and characterization of the central component of the phycobilisome core of Nostoc sp. Plant Physiol 70:1060–1065.

    Google Scholar 

  161. Zilinskas BA and Glick RE (1981) Noncovalent intermolecular forces in phycobilisomes of Porphyridium cruentum. Plant Physiol. 68:447–452.

    Google Scholar 

  162. Zilinskas BA, Grabowski J and Campbell S (1984) Phycoerythrin: spectroscopic analysis of its subunits and aggregates from monomer to dodecamer. In Sybesma C, ed. Advances in Photosynthesis Research, Vol II, pp. 687–690. The Hague: Nijhoff/Junk.

    Google Scholar 

  163. Zilinskas BA and Howell DA (1983) Role of the colorless polypeptides in phycobilisome assembly in Nostoc sp. Plant Physiol 71:379–387.

    Google Scholar 

  164. Zilinskas BA and Howell DA (1985) The immunologically-conserved phycobilisome-thylakoid linker polypeptide. Plant Physiol, in press.

  165. Zilinskas BA, Zimmerman BK and Gantt E (1978) Allophycocyanin forms isolated from Nostoc sp. phycobilisomes. Photochem Photobiol 27:587–595.

    Google Scholar 

  166. Zuber H (1978) Studies on the structure of the light-harvesting pigment-protein complexes from cyanobacteria and red algae. Ber Deutsch Bot Ges Bd 91:459–475.

    Google Scholar 

  167. Zuber H (1985) Structural organization of tetrapyrrole pigments in light-harvesting pigment-protein complexes. In Blauer G and Sund H, eds. Optical Properties and Structure of Tetrapyrroles, pp. 425–441. New York: Walter de Gruyter and Co.

    Google Scholar 

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Zilinskas, B.A., Greenwald, L.S. Phycobilisome structure and function. Photosynth Res 10, 7–35 (1986). https://doi.org/10.1007/BF00024183

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