Photosynthesis Research

, Volume 60, Issue 2–3, pp 111–150

The role of trace metals in photosynthetic electron transport in O2-evolving organisms

  • John A. Raven
  • Michael C. W. Evans
  • Rebecca E. Korb
Article

Abstract

Iron is the quantitatively most important trace metal involved in thylakoid reactions of all oxygenic organisms since linear (= non-cyclic) electron flow from H2O to NADP+ involves PS II (2–3 Fe), cytochrome b6-f (5 Fe), PS I (12 Fe), and ferredoxin (2 Fe); (replaceable by metal-free flavodoxin in certain cyanobacteria and algae under iron deficiency). Cytochrome c6 (1 Fe) is the only redox catalyst linking the cytochrome b6-f complex to PS I in most algae; in many cyanobacteria and Chlorophyta cytochrome c6 and the copper-containing plastocyanin are alternatives, with the availability of iron and copper regulating their relative expression, while higher plants only have plastocyanin. Iron, copper and zinc occur in enzymes that remove active oxygen species and that are in part bound to the thylakoid membrane. These enzymes are ascorbate peroxidase (Fe) and iron-(cyanobacteria, and most al gae) and copper-zinc- (some algae; higher plants) superoxide dismutase. Iron-containing NAD(P)H-PQ oxidoreductase in thylakoids of cyanobacteria and many eukaryotes may be involved in cyclic electron transport around PS I and in chlororespiration. Manganese is second to iron in its quantitative role in the thylakoids, with four Mn (and 1 Ca) per PS II involved in O2 evolution. The roles of the transition metals in redox catalysts can in broad terms be related to their redox chemistry and to their availability to organisms at the time when the pathways evolved. The quantitative roles of these trace metals varies genotypically (e.g. the greater need for iron in thylakoid reactions of cyanobacteria and rhodophytes than in other O2-evolvers as a result of their lower PS II:PS I ratio) and phenotypically (e.g. as a result of variations in PS II:PS I ratio with the spectral quality of incident radiation).

calcium copper iron manganese oxygen evolution phylogeny zinc 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen JF (1993) Redox control of gene expression and the function of chloroplast genomes - an hypothesis. Photosynth Res 36: 950-102Google Scholar
  2. Arisi A-CM, Cornic G, Jouanin L and Foyer CH (1998) Overexpression of iron superoxide dismutase in transformed poplar modifies the regulation of photosynthesis at low CO2 partial pressures or following exposure to the preoxidant herbicide methyl viologen. Plant Physiol 117: 565–574Google Scholar
  3. Arudchandran A, Seeburg D, Burkhart W and Bullerjahn GS (1994) Nucleotide sequence of the pet E gene encoding plastocyanin from the photosynthetic prokaryote, Prochlorothrix hollandica. Biochim Biophys Acta 1188: 447–449Google Scholar
  4. Asada K (1992) Ascorbate peroxidase - a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85: 235–241Google Scholar
  5. Asada K and Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 227–287. Elsevier, AmsterdamGoogle Scholar
  6. Asada K, Kanematsu S and Uchida K (1977) Superoxide dismutases in photosynthetic organisms: Absence of CuZn enzyme in eukaryotic algae. Arch Biochem Biophys 179: 243–256Google Scholar
  7. Asada K, Kanematsu S, Okada S and Hayakana T (1980) Phylogenetic distribution of three types of superoxide dismutase in organisms and in cell organelles. In: Bannister JV and Hill HAO (eds) Chemical and Biochemical Aspects of Superoxide and Superoxide Dismutase, pp 136–153. Elsevier, New YorkGoogle Scholar
  8. Asada K, Heber U and Schreiber U (1993a) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as detected in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol 34: 39–50Google Scholar
  9. Asada K, Miyake C, Sano S and Amako K (1993b) Scavenging of hydrogen peroxide in photosynthetic organisms - from catalase to ascorbate peroxidase. In: Kellinder KG, Rasmusssen SK, Penel C and Greppin H (eds) Plant Peroxidases: Biochemistry and Physiology, pp 243–250. University of GenevaGoogle Scholar
  10. Avelange M-H and Rebeille F (1991) Mass spectrometric demonstration of O2 gas exchange during a dark-to-light transition in higher plant cells. Evidence for two individual O2-uptake components. Planta 183: 158–165Google Scholar
  11. Avellano JB, Schröder WP, Sandmann G, Chueca A and Barón M (1994) Removal of nuclear contaminants and non-specifically Photosystem II-bound copper from Photosystem II preparations. Physiol Plant 91: 369–374Google Scholar
  12. Badger MR (1985) Photosynthetic oxygen exchange. Annu Rev Plant Physiol 36: 27–53Google Scholar
  13. Behrenfeld MJ and Kolber ZS (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283: 840–843Google Scholar
  14. Belkhodja R, Morales F, Quilez R, Lopez Millan AF, Abadia A and Abadia J (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the Photosystem II acceptor. Photosynth Res 56: 265–276Google Scholar
  15. Bendall DS and Manusso RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229: 23–38Google Scholar
  16. Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci 79: 4252–4256Google Scholar
  17. Bennoun P (1993) Effects of mutations and of ionophores on chlororespiration in Chlamydomonas reinhardtii. FEBS Lett 156: 363–365Google Scholar
  18. Bennoun P (1994) Chlororespiration revisited: mitochondrial-plastid interactions in Chlamydomonas. Biochim Biophys Acta 1186: 59–66Google Scholar
  19. Berger S, Ellersiek U, Westhoff P and Steinmüller K (1993) Studies on the expression of NDH-H, a subunit of the NAD(P)H-plastoquinone-oxidoreductase of higher plant chloroplasts. Planta 190: 25–31Google Scholar
  20. Berges JA, Charlebois DO, Mauzerall DG and Falkowski PG (1996) Differential effect of nitrogen limitation on the photosynthetic efficiencies of Photosystems I and II in microalgae. Plant Physiol 110: 689–696Google Scholar
  21. Berry MC, Bratt PJ and Evans MCW (1997) Relaxation properties of the Photosystem I electron transfer components: Indications of the relative position of the electron transfer cofactors in Photosystem I. Biochim Biophys Acta 1319: 163–176Google Scholar
  22. Bhattacharya D and Medlin L (1998) Algal phylogeny and the origin of land plants. Plant Physiol 116: 9–15Google Scholar
  23. Biehle K and Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol 112: 265–272Google Scholar
  24. Blubaugh DJ and Govindjee (1988) The molecular mechanisms of the bicarbonate effect at the plastoquinone reductase site of photosynthesis. Photosynth Res 19: 85–128Google Scholar
  25. Brand LC (1991) Minimum iron requirement of marine phytoplankton and the implications for the biogeochemical control of new production. Limnol Oceanogr 36: 1756–1771Google Scholar
  26. Brandt U (1997) Proton translocation by membrane-bound NADH: Ubiquinone oxidoreductase (complex I) through redox-gated ligand conduction. Biochim Biophys Acta 1318: 79–91Google Scholar
  27. Bruce D, Vidaver W, Colbow K and Popovic R (1983) Electron transport-dependent chlorophyll a-fluorescence quenching by O2 in various algae and higher plants. Plant Physiol 73: 886–888Google Scholar
  28. Büchel C and Garab G (1995) Evidence for the operation of a cyanide-sensitive oxidase in chlororespiration in the thylakoids of the chlorophyll c-containing alga Pleurochloris meiringensis. (Xanthophyceae). Planta 197: 69–75Google Scholar
  29. Büchel C, Zsíros O and Garab G (1998) Alternative cyanidesensitive oxidase interacting with photosynthesis in Synechocystis PCC6803. Ancestor of the terminal oxidase of chlororespiration? Photosynthetica 35: 223–231Google Scholar
  30. Bullerjahn GS and Post AF (1993) The prochlorophytes: Are they more than just chlorophyll a/b containing cyanobacteria? CRC Crit Revs Micro 19: 43–59Google Scholar
  31. Burger-Wiersma T and Matthijis HCP (1990) The Biology of the Prochlorales. In: Codd GA (ed) Autotrophic Microbiology and One-Carbon Metabolism, pp 1–24. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  32. Burrows PA, Sazanov LA, Svab Z, Maliga P and Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868–876Google Scholar
  33. Butow BJ, Wynne D and Tel-Or E (1997) Superoxide dismutase activity in Peridinium gatunense in Lake Kinneret: Effect of light regime and carbon dioxide concentration. J Phycol 33: 787–793Google Scholar
  34. Caron L, Berkaloff C, Duval, J-C and Jupin H (1986) Chlorophyll fluorescence transients from the diatom Phaeodactylum tricornutum: Relative rates of cyclic phosphorylation and chlororespiration. Photosynth Res 10: 131–139Google Scholar
  35. Caron L, Mortain-Bertrand A and Jupin H (1988) Effect of photoperiod on photosynthetic characteristics of two marine diatoms. J Exp Mar Biol Ecol 123: 211–226Google Scholar
  36. Casper-Lindley C and Björkman O (1997) Nigericin insensitive post-illumination reduction in fluorescence yield in Dunaliella tertiolecta (Chlorophyta). Photosynth Res 50: 209–222Google Scholar
  37. Cavalier-Smith T (1982) The origin of plastids. Biol J Linn Soc 17: 289–306Google Scholar
  38. Cavalier-Smith T (1992) The number of symbiotic origins of organelles. Biosystems 28: 91–106Google Scholar
  39. Cha Y and Mauzerall DC (1992) Energy storage as linear and cyclic electron flows in photosynthesis. Plant Physiol 100: 1869–1877Google Scholar
  40. Chase Z and Price NM (1997) Metabolic consequences of iron deficiency in heterotrophic marine protozoa. Limnol Oceanogr 42: 1673–1684Google Scholar
  41. Cheeseman, JM, Herendeen LB, Cheeseman AT and Clough BF (1997) Photosynthesis and photoprotection in mangroves under field conditions. Plant Cell Environm 20: 579–588Google Scholar
  42. Chow WS and Anderson JM (1987) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. II Thylakoid membrane components. Aust J Plant Physiol 14: 9–19Google Scholar
  43. Chow WS, Anderson JM and Melis A (1990a) The Photosystem stoichiometry in thylakoids of some Australian shade-adapted species. Aust J Plant Physiol 17: 665–674Google Scholar
  44. Chow WS, Goodchild DJ, Miller CI and Anderson JM (1990b) The influence of high levels of brief or prolonged supplementary far-red illumination during growth on the photosynthetic characteristics, composition and morphology of Pisum sativum chloroplasts. Plant Cell Environ 13: 135–145Google Scholar
  45. Clarke AK and Campbell D (1996) Inactivation of thePet E gene for plastocyanin lowers photosynthetic capacity and exacerbates chilling induced photoinhibition - in the cyanobacterium Synechococcus. Plant Physiol 112: 1551–1561Google Scholar
  46. Cleaves HJ and Miller SL (1998) Oceanic protection of prebiotic organic compounds from UV radiation. Proc Natl Acad Sci 95: 7260–7263Google Scholar
  47. Collén J (1994) Production of hydrogen peroxide and volatile hydrocarbons by macroalgae. Acta Universitas Upsaliensis, UppsalaGoogle Scholar
  48. Collén J and Pedersén M(1996) Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur J Phycol 31: 265–271Google Scholar
  49. Couture M, Chamberland H, St-Pierre B and Guertin M (1994) Nuclear gene encoding chloroplast hemoglobins in the unicellular green algae Chlamydomonas eugametos. Mol Gen Genet 243: 185–187Google Scholar
  50. Cramer WA, Soriano GM, Ponomarev M, Huang D, Zhang H, Martinez SE and Smith JL (1996) Some new structural aspects and old controversies concerning the cytochrome b 6-f complex of oxygenic photosynthesis. Annu Rev Plant Physiol and Plant Mol Biol 47: 477–508Google Scholar
  51. Cunningham FX Jr, Dennenberg RS, Mustardy L, Jursinic PA and Gantt E. (1989) Stoichiometry of Photosystem I, Photosystem II and phycobilisomes in the red alga Porphydridium cruentum as a function of growth irradiance. Plant Physiol 91: 1179–1187Google Scholar
  52. Darrouzet E, Issartel J-P, Lunardi J and Dupuis A (1998) The 49-kDa subunit of NADH-ubiquinone oxidoreductase (Complex I) is involved in the binding of piericidin and retenone, two quinone-related inhibitors. FEBS Lett 431: 34–38Google Scholar
  53. de Jesus MD, Tabatabai F and Chapman DJ (1989) Taxonomic distribution of copper-zinc superoxide dismutase in green algae and its phylogenetic importance. J Phycol 24: 767–772Google Scholar
  54. de Pamphilis CW and Palmer JD (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348: 337–339Google Scholar
  55. Diner BA and Petrouleas V (1988) Q400, the non-haem iron of the Photosystem II iron-quinone complex. Biochim Biophys Acta Acta 985: 107–125Google Scholar
  56. Droppa M and Horváth G (1990) The role of copper in photosynthesis. CRC Crit Rev Plant Sci 9: 111–123Google Scholar
  57. Droppa M, Terry N and Horváth G (1984) Effects of Cu deficiency on photosynthetic electron transport. Proc Natl Acad Sci USA 81: 2369–2273Google Scholar
  58. Dubinsky Z, Falkowski PG and Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27: 1335–1349Google Scholar
  59. Eiler JN, Mojzsis SJ and Arrhenius G (1997) Carbon isotope evidence for early life. Nature 386: 665Google Scholar
  60. Endo T and Asada K (1996) Dark induction of the non-photochemical quenching of chlorophyll fluorescence by acetate in Chlamydomonas reinhardtii. Plant Cell Physiol 37: 551–555Google Scholar
  61. Endo T, Mi H, Shikanai T and Asada K (1997a) Donation of electrons to plastoquinone by NAD(P)H dehydrogenase and by ferredoxin-quinone reductase in spinach chloroplasts. Plant Cell Physiol 38: 1272–1277Google Scholar
  62. Endo T, Shikanai T, Hashimoto T, Yamada Y, Yokota A and Asada K (1997b) Cyclic electron transport mediated by NAD(P)H dehydrogenase in tobacco chloroplasts. Plant Cell Physiol 38: S527Google Scholar
  63. Endo T, Shikanai T, Sato F and Asada K (1998) NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron donation to plastoquinone in tobacco chloroplasts. Plant Cell Physiol 39: 1226–1231Google Scholar
  64. Eshdat Y, Holland D, Faltin Z and Ben-Hayyim G (1997) Plant glutathione reductases. Physiol Plant 100: 234–240Google Scholar
  65. Evans EH, Rush JD, Johnson CE, Evans MCW and Dickson DPE (1981) The nature of centre X of Photosystem I reaction centres from the cyanobacterium Chlorogloea fritschii determined by Mossbauer spectrometry. Eur J Biochem 118: 81–84Google Scholar
  66. Evans JR (1996) Developmental constraints on photosynthesis: Effects of light and nutrition. In: Baker NR (eds) Photosynthesis and the Environment, pp 281–304. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  67. Evans MCW and Nugent JHA (1993) Structure and function of the reaction centre cofactors of oxygenic organisms. In: Norris JR and Diesenhoffer J (eds) The Photosynthetic Reaction Center, Vol I, pp 391–415. Academic Press, New YorkGoogle Scholar
  68. Evans PK and Krogmann DW (1983) Three c-type cytochromes from the red alga Porphyridium cruentum. Arch Biochem Biophys 227: 494–510Google Scholar
  69. Eyster C (1964) Micronutrient requirements for green plants, especially algae. In: Jackson DF (ed) Algae and Man, pp 86–119. Plenum Press, New YorkGoogle Scholar
  70. Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on biological sequestration of CO2 in the ocean. Nature 387: 272–275Google Scholar
  71. Falkowski PG and Owens TG (1980) Light-shade adaptation. Two strategies of marine phytoplankton. Plant Physiol 66: 592–595Google Scholar
  72. Falkowski PG and Raven JA (1997) Aquatic Photosynthesis. Blackwell Science, Malden, MAGoogle Scholar
  73. Falkowski PG, Owens TG, Ley AC and Mauzerall DC (1981) Effects of growth irradiance on the ratio of reaction centres in two species of marine phytoplankton. Plant Physiol 68: 969–973Google Scholar
  74. Falkowski PG, Dubinsky Z and Wyman K (1985) Growth-irradiance relationships in phytoplankton. Limnol Oceanogr 30: 311–321Google Scholar
  75. Falkowski PG, Sukenik A and Herzig R (1989) Nitrogen limitation of Isochrysis galbana (Haptophyceae). II. Relative abundance of chloroplast proteins. J Phycol 25: 471–478Google Scholar
  76. Falkowski PG, Barber RT and Smetack V (1998) Biogeochemical controls and feedbacks on ocean primary productivity. Science 281: 200–206Google Scholar
  77. Feild TS, Nedbal L and Ort DR (1998) Nonphotochemical reduction of the plastiquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol 116: 1209–1218Google Scholar
  78. Fork DC and Herbert SK (1993) Electron transport and photophosphorylation by Photosystem I in vivo in plants and cyanobacteria. Photosynth Res 36: 149–168Google Scholar
  79. Friedmann AL and Alberte RS (1986) Biogenesis and light regulation of the major light harvesting chlorophyll-protein complexes of diatoms. Plant Physiol 80: 43–51Google Scholar
  80. Fujita Y, Murakami A and Ohki K (1987) Regulation of photosystem composition in the cyanobacterial photosynthetic system: The regulation occurs in response to the redox state of the electron pool located between the two Photosystems. Plant Cell Physiol 28: 283–292Google Scholar
  81. Funk E, Schäfer E and Steinmüller K (1999) Characterization of the complex 1-homologous NAD(P)H-plastoquinoneoxidoreductase (NDH-complex) of maize chloroplasts. J Plant Physiol 154: 16–23Google Scholar
  82. Godde D (1982) Evidence for a membrane bound NADH-plastiquinone-oxidoreductase in Chlamydomonas reinhardtii. Arch Microbiol 131: 197–202Google Scholar
  83. Golbeck JH (1992) Structure and function of Photosystem I. Annu Rev Plant Physiol and Plant Mol Biol 43: 293–324Google Scholar
  84. Goyal A and Tolbert NE (1996) Association of glycolate oxidation with photosynthetic electron transport in plant and algal chloroplasts. Proc Natl Acad Sci USA 93: 3319–3324Google Scholar
  85. Greene RM and Gerard VA (1990) Effects of high-frequency light fluctuation on growth and photoacclimation of the red alga Chondrus crispus. Mar Biol 105: 357–364Google Scholar
  86. Greene RM, Geider RJ and Falkowski PG (1991) Effect of iron limitation on photosynthesis in a marine diatom. Limnol Oceanogr 36: 1772–1782Google Scholar
  87. Groom Q, Kramer DM, Crofts AR and Ort DR (1993) The nonphotochemical reduction of plastoquinone in leaves. Photosynth Res 36: 205–215Google Scholar
  88. Guedeney G, Corneille S, Cuine S and Peltier G (1996) Evidence for association of ndhB, ndhJ gene products and ferredoxin-NADP-reductase as components of a chloroplastic NAD(P)H dehydrogenase complex. FEBS Lett 378: 277–280Google Scholar
  89. Guenther JE, Nemsen JA and Melis A. (1988) Photosystem stoichiometry and chlorophyll antenna size in Dunaliella salina (green algae). Biochim Biophys Acta 934: 108–117Google Scholar
  90. Haberhauser G and Zetschke K (1994) Functional loss of all ndh genes in an otherwise relatively unaltered plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Plant Mol Biol 24: 217–222Google Scholar
  91. Halliwell B and Gutteridge JMC (1989) Free Radicals in Biology and Medicine, second edition. Oxford University Press, OxfordGoogle Scholar
  92. Hankamer B, Barber J and Boekema EJ (1997) Structure and membrane organization of Photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48: 641–671Google Scholar
  93. Harrison PJ, Yu PW, Thompson PA, Price NM and Phillips DJ (1988) Survey of selenium requirements in marine phytoplankton. Mar Ecol Prog Ser 47: 89–96Google Scholar
  94. Heath RL (1972) Light requirements for H+ transport by isolated chloroplast as measured by the bromocresol purple indicator. Biochim Biophys Acta 256: 645–655Google Scholar
  95. Heber U and Walker DA (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol 100: 1621–1626Google Scholar
  96. Heber U, Bukhov NG, Neimanis S and Kobayashi Y (1995a) Maximum H+/hυPSI stoichiometry of proton transport during cyclic electron transport in intact chloroplasts is at least two, but probably higher than two. Plant Cell Physiol 36: 1639–1647Google Scholar
  97. Heber U, Gerst U, Krieger A, Niemanis S and Kibayashi Y (1995b) Coupled cyclic electron transport in intact chloroplasts and leaves of C3 plants. Does it exist? If so, what is its function? Photosynth Res 46: 269–275Google Scholar
  98. Henley WJ and Yin Y (1998) Growth and photosynthesis of marine Synechococcus (Cyanophyceae) under iron stress. J Phycol 34: 94–103Google Scholar
  99. Henry LEA, Halliwell B and Hall DO (1976) The superoxide dismutase activity of various organisms measured by a new and rapid assay technique. FEBS Lett 66: 303–306Google Scholar
  100. Henzler T and Steudle E (1998) Water and solute permeability across water channels. J Exp Bot 49: 105Google Scholar
  101. Herbert SK, Fork DC and Malkin S (1990) Photoaccoustic measurements of in vivo energy storage by cyclic electron flow in algae and higher plants. Plant Physiol 94: 926–934Google Scholar
  102. Hewett-Emmett D and Tashian RE (1996) Functional diversity, conservation and convergence in the evolution of the α-, β-and δ-carbonic anhydrase gene families. Mol Phylogenetics Evol 5: 50–77Google Scholar
  103. Hewitt EJ (1983) A perspective on mineral nutrition: Essential and functional minerals in plants. In: Robb PA and Pierpoint WB (eds) Metals and Micronutrients: Uptake and Utilization by Plants, pp 277–323. Academic Press, LondonGoogle Scholar
  104. Hihara Y, Sonoike K and Ikeuchi M (1998) A novel gene, pmgA, specifically regulates Photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803 in response to high light. Plant Physiol 117: 1205–1216Google Scholar
  105. Hill R and Bendall F (1960) Function of two cytochrome components in chloroplasts: A working hypothesis. Nature 186: 136–137Google Scholar
  106. Hippler H, Redding K and Rochaix J-D (1998) Chlamydomonas genetics, a tool for the study of bioenergetic pathways. Biochim Biophys Acta 1367: 1–62Google Scholar
  107. Hoefnagel MHN, Atkin OK and Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1366: 235–255Google Scholar
  108. Hoganson CW and Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953–1956Google Scholar
  109. Hope AB (1993) The chloroplast cytochrome bf complex: A critical focus on function. Biochim Biophys Acta 1143: 1–22Google Scholar
  110. Howitt CA, Whelan J, Price GD and Day DA (1996) Cloning, analysis and inactivation of the ndhK gene encoding a subunit of NADH quinone oxidoreductase from Anabaena PCC 7120. Eur J Biochem 240: 173–180Google Scholar
  111. Hulsebosch RJ, Allaklendiev SI, Klimov VV, Picord R and Hoff AJ (1998) Effect of bicarbonate on the S2 multiline EPR signal of the oxygen-evolving complex in Photosystem II membrane fragments. FEBS Lett 424: 146–148Google Scholar
  112. Hutchins DA (1995) Iron and the marine phytoplankton community. Prog Phycol Res11: 1–49Google Scholar
  113. Iglesias-Prieto R and Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Biol 113: 163–175Google Scholar
  114. Imsande J (1998) Iron, sulfur, and chlorophyll deficiencies: A need for an integrative approach in plant physiology. Physiol Plant 103: 139–144Google Scholar
  115. Iwamoto K and Ikawa T (1997) Glycolate metabolism and subcellular distribution of glycolate oxidase in Spatoglossum pacificum (Phaeophyceae, Chromophyta). Phycol Res 45: 77–83Google Scholar
  116. Iwata S, Lee JW, Okada K, Lee JK, Iwata M, Rasmussen B, Link TA, Ramaswarmy S and Jap BK (1998) Complete structure of the 11-subunit bovine mitochondrial cytochrome bc 1 complex. Science 281: 64–71Google Scholar
  117. Kana TM (1990) Light-dependent oxygen cycling measured by an oxygen-18 isotope dilution method. Mar Ecol Prog Ser 64: 293–300.Google Scholar
  118. Kana TM (1992) Relationship between photosynthetic oxygen cycling and carbon assimilation in Synechococcus WH 7803 (Cyanophyta). J Phycol 28: 304–308Google Scholar
  119. Kana TM (1993) Rapid oxygen cycling in Trichodesmium thiebautii. Limnol Oceanogr 38: 18–24Google Scholar
  120. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakasaki N, Nanio K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yarrada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136Google Scholar
  121. Karlson J, Clarke A, Chen Z, Mason CB, Moroney JV and Samuelsson G (1996) Chloroplastic carbonic anhydrase of Chlamydomonas reinhardtii: Molecular cloning, sequencing and Western blot analysis of high Ci-requiring mutants. In: Melkonian M (ed) Abstracts of the First European Phycological Congress Cologne, August 1996. Abstract 248, p 36Google Scholar
  122. Karlson J, Clarke A, Chen Z, Hugghins SY, Park YI Husic HD, Moroney JV and Samuelsson G (1998) A novel α-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17: 1208–1216Google Scholar
  123. Kerfeld CA and Krogmann DW(1998) Photosynthetic cytochromes c in cyanobacteria, algae and plants. Annu Rev Plant Physiol and Plant Mol Biol 49: 397–425Google Scholar
  124. Kirk JTO (1994) Light and Photosynthesis in Aquatic Ecosystems, second edition. Cambridge University Press, CambridgeGoogle Scholar
  125. Klimov VV, Baranov SV and Allaklendiev SI (1997) Bicarbonate protects the donor side of Photosystem II against photoinhibition and thermoinactivation. FEBS Lett 418: 243–246Google Scholar
  126. Klöck G, Sültemeyer DF, Fock HP and Kreuzberg K (1989) Gas exchange in intact isolated chloroplasts from Chlamydomonas reinhardtii during starch degradation in the dark. Physiol Plant 75: 109–113Google Scholar
  127. Klugehammer B, Sültemeyer D, Badger MR and Price GD (1997) Analysis of the CO2 concentrating mechanism in the marine cyanobacterium, Synechococcus PCC7002: The role of NdhD3, forming part of a NADH dehydrogenase complex. Abst 13th Annual Meeting Australian Society for Phycology and Aquatic Botany, Hobart, 22-24 January, 1997, pp 80–81Google Scholar
  128. Krieger A and Rutherford AW (1997) Comparison of chloride-depleted and calcium-depleted Photosystem II: The midpoint potential of QA and susceptibility to photodamage. Biochim Biophys Acta 1319: 91–98Google Scholar
  129. Kubicki A, Fuuk E, Westhoff P and Steinmüller K (1996) Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex-I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. Planta 199: 276–281Google Scholar
  130. Kübler JE and Davison IR (1993) Thermal acclimation of light-use characteristics of Chondrus crispus (Rhodophyta). Eur J Phycol 30: 189–195Google Scholar
  131. Kudo I and Harrison PJ (1997) Effect of iron nutrition on the marine cyanobacterium Synechococcus grown on different N sources and irradiances. J Phycol 33: 232–240Google Scholar
  132. La Roche J, Boya PW, McKay RML and Geider RJ (1996) Flavodoxin as an in situmarker for iron stress in phytoplankton. Nature 382: 802–805Google Scholar
  133. Latimer MJ, Derose VJ, Mukerji I, Yachandra VK, Sauer K and Klein MP (1995) Evidence for the proximity of calcium to the manganese cluster of Photosystem II: Determination by x-ray absorption spectroscopy. Biochem 34: 10898–10909Google Scholar
  134. Lawlor DW (1993) Photosynthesis: Molecular, Physiological and Environmental Processes, second edition. Longman Scientific and Technical, HarlowGoogle Scholar
  135. Lee SC and Berry MJ (1996) Knowing when not to stop: Selenocysteine incorporation in eukaryotes. Trends Biochem Sci 21: 203–205Google Scholar
  136. Lee WJ and Whitmarsh J (1989) Photosynthetic apparatus of pea thylakoid membranes. Response to growth light intensity. Plant Physiol 89: 932–940Google Scholar
  137. Li Q and Canvin DT (1998) Energy source for HCO3 - and CO2 transport in air-grown cells of Synechococcus UTEX 625. Plant Physiol 116: 1125–1132Google Scholar
  138. MacLachlan DJ, Nugent JHA and Evans MCW (1994a) A XANES study of the manganese complex of inhibited PS II membrane indicates manganese redox changes between the modified S1, S2 and S3 states. Biochim Biophys Acta 1185: 103–111Google Scholar
  139. MacLachlan DJ, Nugent JHA, Bratt PJ and Evans MCW (1994b) The effects of calcium depletion on the O2-evolving complex in spinach PS II. Biochim Biophys Acta 1186: 186–200Google Scholar
  140. Maden BEH (1995) No soup for starters? Autotrophy and the origin of metabolism. Trends Ecol 10: 111–116Google Scholar
  141. Maldonado MT and Price NM (1996) Influence of N substrate on Fe requirements of marine centric diatoms. Mar Ecol Prog Ser 141: 161–172Google Scholar
  142. Malkin S and Canaani O (1994) The use and characteristics of the photoaccoustic method in the study of photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45: 493–526Google Scholar
  143. Malkin S, Herbert SK and Fork DC (1990) Light distribution, transfer and utilization in the marine red alga Porphyra perforata from photoaccoustic energy-storage measurements. Biochim Biophys Acta 1016: 177–189Google Scholar
  144. Mancinelli RL and McKay CP (1988) The evolution of nitrogen cycling. Origin Life Evolution Biosphere 18: 311–325Google Scholar
  145. Manna P and Vermaas W (1997) Lumenal proteins involved in respiratory electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 35: 407–416Google Scholar
  146. Mano S, Yamaguchi K, Hayashi M and Nishimura M (1997) Stromal and thylakoid-bound ascorbate peroxidases are produced by alternative splicing in pumpkin. FEBS Lett 413: 21–26Google Scholar
  147. Manodori A and Melis A (1987) Cause and effect relationship between environmental conditions and photosystem stoichiometry in Synechococcus 6301. In: Biggins J (ed) Progress in Photosynthesis Research, Volume II, pp 249–252. Nijhoff, Dordrecht, The NetherlandsGoogle Scholar
  148. Marschner H (1995) Mineral Nutrition of Higher Plants, second edition. Academic Press, LondonGoogle Scholar
  149. Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M and Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162–165Google Scholar
  150. Mathai JC and Sitavaman V (1994) Stretch sensitivity of transmembrane mobility of hydrogen peroxide through voids in the bilayer. Role of cardiolipin. J Biol Chem 269: 17784–17793Google Scholar
  151. Matsuo M, Endo T and Asada K (1997) Purification of NAD(P)H dehydrogenase complex (NDH) in Synechocystis PCC6803. Plant Cell Physiol 38: 528Google Scholar
  152. Matsuo M, Endo T and Asada K (1998) Properties of the respiratory NAD(P)H dehydrogenase isolated from the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 39: 263–267Google Scholar
  153. Meisch H-U and Bielig H-J (1975) Effect of vanadium on growth, chlorophyll formation and iron metabolism in unicellular green algae. Arch Microbiol 105: 77–82Google Scholar
  154. Meisch H-U, Hoffmann H and Reinle W (1978) Vanadium catalysis in the nonenzymatic transamination of δ-aminolevulinic acid. Z Naturforsch 33C: 623–628Google Scholar
  155. Merchant S and Dreyfuss BW (1998) Post-translational assembly of photosynthetic metalloproteins. Annu Rev Plant Physiol Plant Mol Biol 49: 25–51Google Scholar
  156. Messinger J, Nugent JHA and Evans MCW (1997) Detection of an epr multiline signal for the S0 state in Photosystem II. Biochem 36: 11055–11060Google Scholar
  157. Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992a) Electron donation from cyclic and respiratory flows to the photosynthetic chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC6803. Plant Cell Physiol 33: 1233–1237Google Scholar
  158. Mi H, Endo T, Schreiber U and Asada K (1992b) Donation of electrons from cytosolic components to the intersystem chain in the cyanobacterium Synechococcus sp. PCC7002 as determined by the reduction of P700 +. Plant Cell Physiol 33: 1099–1105Google Scholar
  159. Mi H, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PC 6803. Plant Cell Physiol 36: 661–668Google Scholar
  160. Mi H, Endo T, Matsuo M, Ogawa T and Asada K (1997) Inhibition of NAD(P)H dehydrogenase (NDH) by HQNO in the cyanobacterium Synechocystis PCC6803. Plant Cell Physiol 38: 528Google Scholar
  161. Miyake C and Asada K (1992a) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33: 541–553Google Scholar
  162. Miyake C and Asada K (1992b) Thylakoid-bound ascorbate peroxidase scavenges hydrogen peroxide photoproduced - photoreduction of monodehydroascorbate radical. In: Murata N (ed) Research in Photosynthesis, II, pp 563–566. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  163. Miyake C, Michihata F and Asada K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol 32: 33043Google Scholar
  164. Miyake C, Cao W-H and Asada K (1993) Purification and molecular properties of the thylakoid-bound ascorbate peroxidase in spinach chloroplasts. Plant Cell Physiol 34: 881–889Google Scholar
  165. Miyake C, Schreiber U and Asada K (1995) Ferredoxin-dependent and Antimycin A-sensitive reduction of cytochrome b-559 by far-red light in maize thylakoids; participation of a monodialreducible cytochrome b-559 in cyclic electron flow. Plant Cell Physiol 36: 743–748Google Scholar
  166. Mojzis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP and Friend CRL (1996) Evidence for life on earth before 3800 million years ago. Nature 384: 55–59Google Scholar
  167. Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG and Yee D (1994) Zinc and carbon co-limitation of marine phytoplankton. Nature 369: 740–742Google Scholar
  168. Muggli DL and Harrison PJ (1997) Effects of iron on two oceanic phytoplanktons grown in natural NE subarctic Pacific seawater with no artificial chelaters present. J Exp Mar Biol Ecol 212: 225–237Google Scholar
  169. Mulkidjianian Y and Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis - a primordial UVprotection as common ancestor of reaction centers and antenna proteins. Photosynth Res 31: 27–42Google Scholar
  170. Mullineaux PM, Karpinski S, Jiménez A, Cleary SP, Robinson C and Creisser GP (1998) Identification of cDNAs encoding plastid-targeted glutathione peroxidase. Plant J 13: 375–379Google Scholar
  171. Murakami A, Kim S-J and Fujita Y (1997) Changes in photosystem stoichiometry in response to environmental conditions for cell growth observed with the cyanophyte Synechocystis PCC6714. Plant Cell Physiol 38: 392–397Google Scholar
  172. Navarro JA, Hervas M, De Le Gedra B and De La Rosa MA (1995) Purification and physicochemical properties of the low-potential cytochrome c 549 from the cyanobacterium Synechocystis sp. PCC6803. Arch Biochem Biophys 318: 46–52Google Scholar
  173. Nicholls DG and Ferguson SJ (1992) Bioenergetics 2. Academic Press, LondonGoogle Scholar
  174. Nixon PJ and Maliga P (1999) Chlororespiration: Only half a story. Trends Plant Sci 4: 51Google Scholar
  175. Noctor G and Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol and Plant Mol Biol 49: 249–279Google Scholar
  176. Obinger C, Regelsberger G, Pircher A, Strasser G and Peschek GA (1998) Scavenging of superoxide and hydrogen peroxide in blue-green algae (cyanobacteria). Physiol Plant 104: 693–698Google Scholar
  177. Ogawa T (1991) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803. Proc Natl Acad Sci 88: 4275–4279Google Scholar
  178. Ogawa T, Omata T, Miyano A and Inowe Y (1985) Photosynthetic reactions involved in the CO2-concentrating mechanism in the cyanobacterium, Anacystis nidulans. In: Lucas WJ and Berry JA (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp 287–304. American Society of Plant Physiologists, Rockville, MDGoogle Scholar
  179. Ogawa K, Kanematsu S, Takabe K and Asada K (1995) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PS I) in spinach chloroplasts: detection by immuno-gold labelling after rapid freezing and substitution method. Plant Cell Physiol 36: 565–573Google Scholar
  180. Ohkawa H, Murakami A, Sonoda M and Ogawa T (1998) Analysis of five ndhD mutants of Synechocystis PCC6803. Plant Cell Physiol 39: s19Google Scholar
  181. Okada S, Kanematsu S and Asada K (1979) Intracellular distribution of manganese and ferric superoxide dismutases in blue-green algae. FEBS Lett 103: 106–110Google Scholar
  182. Osmond CB and Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46: 1351–1362Google Scholar
  183. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740Google Scholar
  184. Pakulski JD, Coffin RB, Kelley CA, Holde, SL, Downer R, Aas P, Lyons Mm and Jeffrey WH (1996) Iron stimulation of Antarctic bacteria. Nature 383: 133–134Google Scholar
  185. Partensky F, La Roche J, Wyman K and Falkowski PG (1997) The divinyl-chlorophyll a/b-protein complexes of two strains of the oxyphototrophic marine prokaryote Prochlorococcus - characterization and response to changes in growth irradiance. Photosynth Res 51: 209–222Google Scholar
  186. Patterson COP and Myers T (1973) Photosynthetic production of hydrogen peroxide by Anacystis nidulans. Plant Physiol 51: 104–109Google Scholar
  187. Peltier G and Schmidt GW (1991) Chlororespiration: An adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88: 4791–4795Google Scholar
  188. Pfannschmidt T, Nilsson A and Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625–628Google Scholar
  189. Prosil, O, Kolber Z, Berry JA and Falkowski PG (1996) Cyclic electron flow around PS II in vivo. Photosynth Res 48: 395–410Google Scholar
  190. Price NM and Harrison PJ (1988) Specific selenium-containing macromolecules in the marine diatom Thalassiosira pseudonana. Plant Physiol 86: 192–199Google Scholar
  191. Price NM, Thompson A and Harrison PJ (1987) Selenium: An essential element for growth of the coastal marine diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 23: 1–9Google Scholar
  192. Price NM, von Caemmerer S, Evans JR, Siebke K, Andersen JM and Badger MR (1998) Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco. Aust J Plant Physiol 25: 445–452Google Scholar
  193. Radmer RK and Kok B (1976) Photoreduction of O2 primes and replaces CO2 assimilation. Plant Physiol 58: 336–340Google Scholar
  194. Radmer RK and Ollinger O (1980) Light-driven uptake of oxygen, carbon dioxide and bicarbonate by the green alga Scenedesmus. Plant Physiol 65: 723–729Google Scholar
  195. Radmer RK and Ollinger O (1981) The variability of light-driven oxygen uptake in algae. Plant Physiol 67: 119.Google Scholar
  196. Radmer RK, Kok B and Ollinger O (1978) Kinetics and apparent Km of O2 cycle under conditions of limiting carbon dioxide fixation. Plant Physiol 61: 915–917Google Scholar
  197. Raven JA (1976a) Division of labour between chloroplasts and cytoplasm. In: Barber J (ed) The Intact Chloroplast, pp 403–443. Elsevier, AmsterdamGoogle Scholar
  198. Raven JA (1976b) Transport in algal cells. In: Lüttge U and Pitman Mg (eds) Transport in Cells and Tissues: Encyclopedia of Plant Physiol, new series, Vol IIA, pp 129–188. Springer-Verlag, BerlinGoogle Scholar
  199. Raven JA (1982) The energetics of freshwater algae; energy requirements for biosynthesis and volume regulation. New Phytol 92: 10–20Google Scholar
  200. Raven JA (1984) Energetics and Transport in Aquatic Plants. A.R. Liss, New YorkGoogle Scholar
  201. Raven JA (1986) Physiological consequences of extremely small size for autotrophic organisms in the sea. In: Platt TR and Li WKW (eds) Photosynthetic Picoplankton, pp 1–70. Canadian Bulletin of Fisheries and Aquatic Sciences 214Google Scholar
  202. Raven JA (1987a) Biochemistry, biophysics and physiology of chlorophyll b-containing algae: Implications for taxonomy and phylogeny. Progr Phycol Res 5: 1–122Google Scholar
  203. Raven JA (1987b) The role of vacuoles. New Phytol 106: 357–422Google Scholar
  204. Raven JA (1988a) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol 109: 279–285Google Scholar
  205. Raven JA (1988b) Algae. In: Baker DA and Hall JL (eds) Solute Transport in Plant Cells and Tissues, pp 166–219. Longman Scientific and Technical, HarlowGoogle Scholar
  206. Raven JA (1990) Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and C assimilation pathway. New Phytol 116: 1–18Google Scholar
  207. Raven JA (1995) Costs and benefits of low intracellular osmolarity in cells of freshwater algae. Funct Ecol 9: 701–707.Google Scholar
  208. Raven JA (1997a) CO2 concentrating mechanisms: A direct role for thylakoid lumen acidification? Plant Cell Environ 20: 147–154Google Scholar
  209. Raven JA (1997b) The role of marine biota in the evolution of terrestrial biota: Gases and genes. Biogeochemistry 39: 139–164Google Scholar
  210. Raven JA (1997c) The vacuole: A cost-benefit analysis. Adv Bot Res 25: 59–86Google Scholar
  211. Raven JA (1997d) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27: 85–209Google Scholar
  212. Raven JA (1998a) Small is beautiful. Funct Ecol 12: 503–513Google Scholar
  213. Raven JA (1998b) Extrapolating feedback processes from the present to the past. Phil Trans R Soc London 353: 19–28Google Scholar
  214. Raven JA (1999) Picophytoplankton. Prog Phycol Res, in pressGoogle Scholar
  215. Raven JA and Yin Z-H (1998) The past, present and future of nitrogenous compounds in the atmosphere and their interactions with plants. New Phytol 139: 205–219Google Scholar
  216. Raven JA, Johnston AM and bin Surif M (1989) The photosynthetic apparatus as a phyletic character. In: Green JC, Leadbeater BSC and Diver WL (eds) The Chromophyte Algae: Problems and Perspectives, pp 63–84. The Systematics Association Special Volume No 33. Clarendon Press, OxfordGoogle Scholar
  217. Raven JA, Johnston AM and MacFarlane JJ (1990) Carbon metabolism. In: Sheath RG and Cole KM (eds) The Biology of the Red Algae, pp 171–202. Cambridge University Press, CambridgeGoogle Scholar
  218. Raven JA, Johnston AM, Kübler JE, and Parsons R (1994) The influence of natural and experimental high O2 concentration on O2-evolving photolithotrophs. Biol Revs 69: 61–94Google Scholar
  219. Regelsberger G, Obinger C, Zoder R, Altman F and Peschek G (1999) Purification and characterization of a hydroperoxidase from the cyanobacterium Synechocystis PCC 6803: Identification of its gene by peptide mass mapping using matrix assisted laser desorption ionization time-of-flight mass spectrometry. FEMS Microbiol Lett 170: 1–12Google Scholar
  220. Reith M (1995) Molecular biology of rhodophyte and chromophyte plastids. Annu Rev Plant Physiol and Plant Mol Biol 46: 549–575Google Scholar
  221. Rhee K-H, Morris EP, Barber J and Kühlbrandt W (1998) Three-dimensional structure of the plant Photosystem II reactive centre at 8Å resolution. Nature 396: 283–286Google Scholar
  222. Rich PR, Hoefnagel MHN and Wiskich JT (1998) Possible chlororespiratory reactions of thylakoid membranes. In: Moeller IM, Gardeström P, Glimelius K and Glaser E (eds) From Gene to Function, pp 17–23. Backhuys Publishers, LeidenGoogle Scholar
  223. Riggs-Gelasco P, Mei R, Yocum CF and Penner-Hahn JE (1996) Reduced derivatives of the Mn cluster in the oxygen evolving complex Photosystem II, an EXAFS study. J Am Chem Soc 118: 2387–2399Google Scholar
  224. Rochaix J-D (1997) Chloroplast reverse genetics: New insights into the function of plastid genes. Trends Plant Sci 2: 419–425Google Scholar
  225. Rögner M, Nixon PJ and Diner BA (1990) Purification and characterization of Photosystem I and Photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC6803. J Biol Chem 265: 6169–6196Google Scholar
  226. Roldán M (1999) Can chlororespiration in plants help to explain the controversial phenotype of ndh mutants? Trends Plant Sci 4: 50Google Scholar
  227. Rosing MT (1999) 13C-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from West Greenland. Science 283: 674–676Google Scholar
  228. Rueter JG (1993) Limitation of primary productivity in the oceans by light, nitrogen and iron. In: Yamamoto HY and Smith CM (eds) Photosynthetic Responses to the Environment, pp. 126–135. American Society for Plant Physiol, Rockville, MDGoogle Scholar
  229. Russell MJ and Hall AJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc London 154: 377–402Google Scholar
  230. Sazanov LA Burrows PA and Nixon PJ (1998a) The plastid ndh genes code for a NADH-specific dehydrogenase: Isolation of a complex 1 analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95: 1319–1324Google Scholar
  231. Sazanov LA, Burrows PA and Nixon PJ (1998b) The chloroplast ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett 429: 115–118Google Scholar
  232. Schäfer G, Purschke W and Schmidt CL (1996) On the origin of respiration: Electron transport proteins from Archaea to man. FEMS Microbiol Revs 18: 173–188Google Scholar
  233. Scheller HV (1996) In vitro cyclic electron transport in barley follows two independent pathways. Plant Physiol 110: 187–194Google Scholar
  234. Scheller HV, Naver H and Moller BL (1997) Molecular aspects of Photosystem I. Physiol Plant 100: 842–851Google Scholar
  235. Scherer S (1990) Do photosynthetic and respiratory electron transport chains share redox proteins? Trends Biochem Sci 15: 458–462Google Scholar
  236. Schidlowski M (1988) A 3,800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333: 313–318Google Scholar
  237. Schluchler WM, Zhao J and Bryant DA (1993) Isolation and characterization of the ndhF gene of Synechococcus sp. PCC7002 and initial characterization of an interposon mutant. J Bacteriol 175: 3343–3352Google Scholar
  238. Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 409–435. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  239. Schomburg D and Stephan D (eds) (1994) Enzyme Handbook, Volume 8. Springer Verlag, BerlinGoogle Scholar
  240. Schomburg D, Salzmann M and Stephan D (eds) (1994) Enzyme Handbook, Volume 7. Springer Verlag, BerlinGoogle Scholar
  241. Schubert WD, Klukas O, Krauss N, Saenger W, Fromme P and Witt HT (1997) Photosystem I of Synechococcus elongatus at 4 Angstrom resolution: A comprehensive structure analysis. JMol Biol 272: 741–769Google Scholar
  242. Shigeoka S, Takeda T and Hanaoka T (1991) Characterization and immunological properties of selenium-containing glutathione peroxidase induced by selenite in Chlamydomonas reinhardtii. Biochem J 275: 623–627Google Scholar
  243. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K and Yokota A (1998a) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around PS I. Proc Natl Acad Sci USA 95: 9705–9709Google Scholar
  244. Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa K-I, Yokota A and Shigeoka S (1998b) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428: 47–51Google Scholar
  245. Siedow JN (1995) Bioenergetics: The mitochondrial electron transfer chain. In: Levings III CS and Vasil IK (eds) The Molecular Biology of Plant Mitochondria, pp 281–312. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  246. Smith BM and Melis A (1987) Photosystem stoichiometry and excitation distribution in chloroplasts from surface and minus 20 m blades of Macrocystis pyrifera, the giant kelp. Plant Physiol 84: 1325–1330Google Scholar
  247. Smith JL (1998) Secret life of cytochrome bc 1. Science 281: 58–59Google Scholar
  248. Smith PM and Melis A (1988) Photosynthetic responses of diatoms to growth irradiance. Plant Physiol 86: 132aGoogle Scholar
  249. Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65: 83–100Google Scholar
  250. Stemler AJ (1997) The case for chloroplast thylakoid carbonic anhydrase. Physiol Plant 99: 348–353Google Scholar
  251. Stewart DH and Brudwig GW(1998) Cytochrome b 559 of photosystem II. Biochim Biophys Acta 1367: 63–87Google Scholar
  252. Stiller JWand Hall BD (1997) The origin of red algae: Implications for plastid evolution. Proc Natl Acad Sci USA 94: 4520–4525Google Scholar
  253. Sukenik A, Bennett J and Falkowski P (1987) Light-saturated photosynthesis-limitation by electron transport or carbon fixation. Biochim Biophys Acta 891: 205–215Google Scholar
  254. Sültemeyer D, Price GD, Bryant DA and Badger MR (1997) PsaE and ndhF mediated electron transport affects bicarbonate transport rather than carbon dioxide uptake in the cyanobacterium Synechococcus sp. PCC 7002. Planta 201: 36–42Google Scholar
  255. Summers DP and Chang S (1993) Prebiotic ammonia from reduction of nitrite by iron (II) on the early earth. Nature 365: 630–633Google Scholar
  256. Sunda WG and Huntsman SA (1986) Relationships among growth rate, cellular manganese concentrations, and manganese transport kinetics in estuarine and oceanic species of the diatom Thalassiosira. J Phycol 22: 259–270Google Scholar
  257. Sunda WG and Huntsman SA (1995a) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem 50: 189–206Google Scholar
  258. Sunda WG and Huntsman SA (1995b) Cobalt and zinc interplacement in marine phytoplankton: Biological and geochemical implications. Limnol Oceanogr 40: 1404–1417Google Scholar
  259. Sunda WG and Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine picophytoplankton growth. Nature 390: 389–392Google Scholar
  260. Sunda WG and Huntsman SA (1998) Interactive effects of external manganese, the toxic metals copper and zinc, and light in controlling cellular manganese and growth in a coastal diatom. Limnol Oceanogr 43: 1467–1475Google Scholar
  261. Sunda WG, Swift DG and Hutchison SA (1991) Low iron requirement for growth in oceanic phytoplankton. Nature 351: 55–57Google Scholar
  262. Suzuki K, Iwamoto K, Yokoyama S, Ikawa T (1991) Glycolateoxidizing enzymes in algae. J Phycol 27: 492–498Google Scholar
  263. Takahashi M-A and Asada K (1983) Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch Biochem Biophys 226: 558–566Google Scholar
  264. Takeda T, Nakano Y and Shigeoka S (1993) Effects of selenite, CO2 and illumination on the induction of selenite-dependent glutathione peroxidase in Chlamydomonas reinhardtii. Plant Sci 94: 81–88Google Scholar
  265. Takeda T, Yokota Y and Shigeoka S (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol 36: 1089–1095Google Scholar
  266. Tanaki Y, Katada S, Ishikawa H, Ogairana T and Takabe T (1997) Electron flow from NAD(P)H dehydrogenase to Photosystem I is required for adaptation to salt shock in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 38: 1311–1318Google Scholar
  267. Teicher HB and Scheller HV (1998) The NAD(P)H dehydrogenase in barley thylakoids is photoactivable and uses NADPH as well as NADH. Plant Physiol 117: 525–532Google Scholar
  268. Tel-Or E, Nuflejt M and Packer L (1985) The role of glutathione and ascorbate in hydroperoxide removal in cyanobacteria. Biochem Biophys Res Commun 132: 533–539Google Scholar
  269. Ting CS and Owens TG (1993) Photochemical and nonphotochemical fluorescence quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol 101: 1323–1330Google Scholar
  270. Tortel PD, Maldonado MT and Price NM (1996) The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383: 330–332Google Scholar
  271. Trissl HW and Wilhelm C (1993) Why do thylakoids from higher plants form membrane stacks? Trends Biochem Sci 18: 415–419Google Scholar
  272. Vallee BL and Galdes A (1984) The metallobiochemistry of zinc enzymes. Advs Enzymol 56: 283–430Google Scholar
  273. van den Hoek C, Mann DG and Jahns HM (1995) Algae: An Introduction to Phycology. Cambridge University Press, CambridgeGoogle Scholar
  274. Van Leeuwe MA, Stefels J and de Baar HJW (1997) The light harvesting capacity of Antarctic phytoplankton remains under iron limitation. Phycologia 34(supplement) 116Google Scholar
  275. Wakao N, Yokoi N, Isoyama N, Hiraishi A, Shimada, K, Kobayashi M, Kise H, Iwaka M, Itoh S, Takaichi S and Sakurai Y (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant Cell Physiol 37: 889–893Google Scholar
  276. Wakasugi T, Tsudzuki T, Shibata M and Hira A (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of black pine (Pinus thungergii). Proc Natl Acad Sci USA 91: 9794–9798Google Scholar
  277. Walker JE (1992) The NADH: ubiquinone oxidoreductase (complex I) of respiratory chains. Quarterly Rev Biophys 25: 253–324Google Scholar
  278. Walls ML, Price NM and Bruland KW (1995) Iron chemistry in seawater and its relationship to phytoplankton: A workshop report. Mar Chem 48: 157–182Google Scholar
  279. Whitehouse DG and Moore AL (1995) Regulation of oxidative phosphorylation in plant mitochondria. In: Levings III CS and Vasil IK (eds) The Molecular Biology of Plant Mitochondria, pp 313–344. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  280. Whitmarsh J, Samson G and Poulson M (1994) Photoprotection in Photosystem II - the role of cytochrome b 559. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis. From Molecular Mechanisms to the Field, pp 75–93. Bios Scientific Publishers, OxfordGoogle Scholar
  281. Wiekkowski S and Bojko M (1997) The NADPH-dependent electron flow in chloroplasts of the higher plants. Photosynthetica 34: 481–496Google Scholar
  282. Wiese C, Shi L-H and Heber V (1998) Oxygen reduction in the Mehler reaction is insufficient to protect Photosystems I and II of leaves against photoactivation. Physiol Plant 102: 437–446Google Scholar
  283. Wilhelm C and Wild A (1984a) The variability of the photosynthetic unit in Chlorella. I. The effect of vanadium on photosynthesis, productivity P-700 and cytochrome f in undiluted and homocontinous cultures of Chlorella. J Plant Physiol 115: 115–124Google Scholar
  284. Wilhelm C and Wild a (1984b) The variability of the photosynthetic unit in Chlorella. II. The effect of light intensity and cell development on photosynthesis, P-700 and cytochrome f in homocontinous and synchronous cultures of Chlorella. J Plant Physiol 115: 125–135Google Scholar
  285. Wilhelm C and Duval J-C (1990) Fluorescence induction kinetics as a tool to detect a chlororespiratory activity in the prasinophycean alga, Mantoniella squamata. Biochim Biophys Acta 1016: 197–202Google Scholar
  286. Wilhelm C, Krämer P and Lenartz-Weiler I (1989) The energy distribution between the photosystems and light-induced changes in the stoichiometry of system I and II reaction centers in the chlorophyll b-containing alga Mantoniella squamata (Prasinophyceae). Photosynth Res 20: 221–233Google Scholar
  287. Wilhelm SW, Maxwell DP and Trick CG (1996) Growth, iron requirements, and siderophore production in iron-limited Synechococcus PCC7002. Limnol Oceanogr 41: 89–97Google Scholar
  288. Williams RJP and FraÚsto da Silva JJR (1996) The Natural Selection of the Chemical Elements. Clarendon Press, Oxford.Google Scholar
  289. Wood PM (1997) The roles of c-type cytochromes in algal photosynthesis: extraction from algae of a cytochrome similar to higher plant cytochrome f. Eur J Biochem 72: 605–613Google Scholar
  290. Yachandra VK, Derose VJ, Latimer MJ, Mukerji I, Sauver K and Klein MP (1993) Where plants make oxygen - a structural model for the photosynthetic oxygen-evolving manganese cluster. Science 260: 675–679Google Scholar
  291. Yocum CF (1991) Calcium activation of photosynthetic water oxidation. Biochim Biophys Acta 1059: 1–15Google Scholar
  292. Yu I, Zhao J, Huhlenhoff V, Bryant DA and Golbeck JH (1993) PsaE is required for in vivo cyclic flow around Photosystem I in the cyanobacterium Synechococcus sp. PCC7002. Plant Physiol 103: 171–180Google Scholar
  293. Yung YL and McElvoy MB (1979) Fixation of nitrogen in the prebiotic atmosphere. Science 203: 1002–1004Google Scholar
  294. Zhang L, Pakrasi HB and Whitmarsh J (1994) Photoautotrophic growth of the cyanobacterium Synechocystis sp. PCC6803 in the absence of cytochrome c553 and plastocyanin. J Biol Chem 269: 5036–5042Google Scholar
  295. Zhao J, Snyder WB, Mühlenhoff U, Rhiel E, Warren PV, Golbeck JH and Bryant DA (1993) Cloning and characterization of the psaE gene of the cyanobacterium Synechococcus sp. PCC7002: Characterization of a psaE mutant and overproduction of the protein in Escherichia coli. Mol Microbiol 9: 183–194Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • John A. Raven
    • 1
  • Michael C. W. Evans
    • 2
  • Rebecca E. Korb
    • 3
  1. 1.Department of Biological SciencesUniversity of DundeeDundeeUK
  2. 2.Department of BiologyUniversity College LondonLondonUK
  3. 3.Marine Sciences Research CenterState University of New YorkStony BrookUSA
  4. 4.Wrigley Institute of Marine SciencesUniversity of Southern CaliforniaUSA

Personalised recommendations