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The cyanobacterium Synechococcus modulates Photosystem II function in response to excitation stress through D1 exchange

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Abstract

In this minireview we discuss effects of excitation stress on the molecular organization and function of PS II as induced by high light or low temperature in the cyanobacterium Synechococcus sp. PCC 7942. Synechococcus displays PS II plasticity by transiently replacing the constitutive D1 form (D1:1) with another form (D1:2) upon exposure to excitation stress. The cells thereby counteract photoinhibition by increasing D1 turn over and modulating PS II function. A comparison between the cyanobacterium Synechococcus and plants shows that in cyanobacteria, with their large phycobilisomes, resistance to photoinhibition is mainly through the dynamic properties (D1 turnover and quenching) of the reaction centre. In contrast, plants use antenna quenching in the light-harvesting complex as an important means to protect the reaction center from excessive excitation.

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Abbreviations

D1:

reaction center protein of Photosystem II

P680 :

the reaction center of Photosystem II

QA :

the primary quinone acceptor of Photosystem II

TyrZ :

tyrosine electron donor to P680

References

  • Andersson B and Styring S (1991) Photosystem II: Molecular organization, function and acclimation. Current Topics in Bioenergetics 16: 1–81

    Google Scholar 

  • Anderson JM and Andersson B (1988) The dynamic photosynthetic membrane and regulation of solar energy conversion. Trends Biochem Sci 13: 352–355

    Google Scholar 

  • Anderson JM and Aro E-M (1994) Grana stacking and protection of Photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: An hypothesis. Photosynth Res 41: 315–326

    Google Scholar 

  • Aro EM, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    Google Scholar 

  • Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66

    Google Scholar 

  • Bouyoub A, Vernotte C and Astier C (1993) Functional analysis of the homologous psbA gene copies in Synechocystis PCC 6714 and PCC 6803. Plant Mol Biol 21: 249–258

    Google Scholar 

  • Bryant DA (1991) Cyanobacterial phycobilisomes: Progress towards complete structural and functional amalysis via molecular genetics. In: Bogorad L and Vasil IK (eds) The Photosynthetic Apparatus: Molecular Biology and Operation Cell Culture and Somatic Cell Genetics of Plants, Vol 7B, pp 257–300. Academic Press, San Diego

    Google Scholar 

  • Bustos SA and Golden SS (1992) Light-regulated expression of the psbD gene family in Synechococcus sp. strain PCC 7942: evidence for the role of duplicated psbD genes in cyanobacteria. Mol Gen Genet 232: 221–230

    Google Scholar 

  • Campbell, D, Bruce D, Carpenter C, Gustafsson P and Öquist G (1995a) Two forms of the Photosystem II D1 protein alter energy dissipation and state transitions in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res (submitted)

  • Campbell D, Zhou G, Gustafsson P, Öquist G and Clarke AK (1995b) Electron transport regulates exchange of two forms of Photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J (in press)

  • Castenholtz RW (1973) Ecology of blue-green algae in hot springs. In: Can NG and Witton BA (eds) The Biology of Blue-Green Algae, pp 379–414. Blackwell, Oxford

    Google Scholar 

  • Clarke AK, Soitamo A, Gustafsson P and Öquist G (1993a) Rapid interchange between two distinct forms of cyanobacterial D1 Photosystem II reaction center protein in response to photoinhibition. Proc Natl Acad Sci USA 90: 9973–9977

    Google Scholar 

  • Clarke AK, Hurry VM, Gustafsson P and Öquist G (1993b) Two functionally distinct forms of the Photosystem II reaction center D1 protein in the cyanobacterium Synechococcus sp. PCC 7942. Proc Natl Acad Sci USA 90: 11985–11989

    Google Scholar 

  • Clarke AK, Campbell D, Gustafsson P and Öquist G (1995) Dynamic responses of Photosystem II and phycobilisomes to changing light in the cyanobacterium Synechococcus sp. PCC 7942. Planta (in press)

  • Curtis SE and Haselkorn R (1984) Isolation, sequence and expression of two members of the 32-kd thylakoid membrane protein gene family from the cyanobacterium Anabaena 7120. Plant Mol Biol 3: 249–255

    Google Scholar 

  • DeLas Rivas J, Andersson B and Barber J (1992) Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in Photosystem II core complexes. FEBS Lett 301: 246–252

    Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for xantophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24

    Google Scholar 

  • Fogg GE, Steward WD, Fay P and Walsby AE (1973) The Blue-Green Alga. Academic Press. London

    Google Scholar 

  • Fork DC and Mohanty P (1986) Fluorescence and other characteristics of blue-green algae (cyanobacteria), red algae and cryptomonads. In: Govindjee, Amesz J and Fork DC (eds) Light Emission by Plants and Bacteria, pp 451–496. Academic Press, London

    Google Scholar 

  • Fujita Y and Murakami A (1987) Regulation of electron transport composition in cyanobacterial photosynthetic system: Stoichiometry among Photosystem I and II complexes and their light-harvesting antennae and cytochrome b 6-f complex. Plant Cell Physiol 28: 1547–1553

    Google Scholar 

  • Gingrich JC, Buzby JS, Stirewalt VL and Bryant DA (1988) Genetic analysis of two new mutations resulting in herbicide resistance in the cyanobacterium Synechococcus sp. PCC 7002. Photosynth Res 16: 83–99

    Google Scholar 

  • Golden SS, Brusslan J and Haselkorn R (1986) Expression of a family of psbA genes encoding a Photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798

    Google Scholar 

  • Golden SS, Cho D-SC and Nalty MS (1989) Two functional psbD genes in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171: 4707–4713

    Google Scholar 

  • Gray MW and Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Miorobiol Rev 46: 1–42

    Google Scholar 

  • Guenther J and Melis A (1990) The physiological significance of Photosystem II heterogenity in chloroplasts. Photosynth Res 23: 105–109

    Google Scholar 

  • Huner NPA, Öquist G, Hurry VM, Krol M, Falk S and Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19–39

    Google Scholar 

  • Jansson C, Debus RJ, Osiewacz HD, Gurevitz M and McIntosh L (1987) Construction of an obligate photoheterotrophic mutant of the cyanobacterium Synechocystis 6803. Plant Physiol 85: 1021–1025

    Google Scholar 

  • Jegerschöld C and Styring S (1990) Fast oxygen-independent degradation of the D1 reaction center protein in Photosystem II. FEBS Lett 269: 45–48

    Google Scholar 

  • Krupa Z, Öquist G and Gustafsson P (1990) Photoinhibition and recovery of photosynthesis in psbA gene-inactivated strains of cyanobacterium Anacystis nidulans. Plant Physiol 93: 1–6

    Google Scholar 

  • Krupa Z, Öquist G and Gustafsson P (1991) Photoinhibition of photosynthesis and growth responses at different light levels in psbA gene mutants of the cyanobacterium Synechococcus. Physiol Plant 82: 1–8

    Google Scholar 

  • Kulkarni RD and Golden SS (1994) Adaptation to high light intensity in Synechococcus sp. strain PCC 7942: Regulation of three psbA genes and two forms of the D1 protein. J Bacteriol 176: 959–965

    Google Scholar 

  • Kulkarni RD, Schaefer MR and Golden SS (1992) Transcriptional and posttranscriptional components of psbA response to high light intensity in Synechococcus sp. strain PCC 7942. J Bact 174: 3775–3781

    Google Scholar 

  • Kyle DJ (1987) The biochemical basis for photoinhibition of Photosystem II. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 197–226. Elsevier, Amsterdam

    Google Scholar 

  • Lidholm J, Szmidt AE and Gustafsson P (1991) Duplication of the psbA gene in the chloroplast genome of two Pinus species. Mol Gen Genet 226: 345–352

    Google Scholar 

  • Maxwell DP, Falk S, Trick CG and Huner NPA (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105: 535–543

    Google Scholar 

  • Miller AG, Espie GS and Canvin DT (1991) The effects of inorganic carbon and oxygen on fluorescence in the cyanobacterium Synechococcus UTEX 625. Can J Bot 69: 1151–1160

    Google Scholar 

  • Mulligan B, Schultes N, Chen L and Bogorad L (1984) Nucleotide sequence of a multiple-copy gene for the B protein of Photosystem II of a cyanobacterium. Proc Natl Acad Sci USA 81: 2693–2697

    Google Scholar 

  • Öquist G (1974) Distribution of chlorophyll between the two photoreactions in photosynthesis of the blue-green alga Anacystis nidulans grown at two different light intensities. Physiol Plant 30: 38–44

    Google Scholar 

  • Öquist G and Huner NPA (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189: 150–156

    Google Scholar 

  • Öquist G, Chow WS and Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of Photosystem II. Planta 186: 450–460

    Google Scholar 

  • Peschek GA (1987) Respiratory electron transport. In: Fay P and VanBaalen C (eds) The Cyanobacteria, pp 119–161. Elsevier, Amsterdam

    Google Scholar 

  • Raven JA (1984) Energetics and Transport in Aquatic Plants. Alan R. Liss, Inc. New York

    Google Scholar 

  • Romero JM, Lara C and Sivak MN (1992) Effect of carbon and nitrogen assimilation on chlorophyll fluorescence emission by the cyanobacterium Anacystis nidulans. Physiol Plant 85: 433–438

    Google Scholar 

  • Samuelsson G, Lönneborg A, Rosenqvist E, Gustafsson P and Öquist G (1995) Photoinhibition and reactivation of photosynthesis in the cyanobacterium Anacystis nidulans. Plant Physiol 79: 992–995

    Google Scholar 

  • Samuelsson G, Lönneborg A, Gustafsson P and Öquist G (1987) The susceptibility of photosynthesis to photoinhibition and the capacity of recovery in high and low light grown cyanobacteria Anacystis nidulans. Plant Physiol 83: 438–441

    Google Scholar 

  • Schaefer MR and Golden SS (1989) Differential expression of members of the psbA gene family in response to light. J Bacteriol 17: 3973–3981

    Google Scholar 

  • Shyam R, Raghavendra AS and Sane PV (1993) Role of dark respiration in photoinhibition of photosynthesis and its reactivation in the cyanobacterium Anacystis nidulans. Physiol Plant 88: 446–452

    Google Scholar 

  • Sundby C, McCaffery S and Anderson JM (1993) Turnover of the Photosystem II D1 protein in higher plants under photoinhibitory and non-photoinhibitory irradiance. J Biol Chem 268: 25476–25482

    Google Scholar 

  • Tandeau de Marsac N and Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: New steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119–190

    Google Scholar 

  • Tsinoremas NF, Schaefer MR and Golden SS (1994) Blue and red light reversibly control psbA expression in the cyanobacterium Synechococcus sp. Strain PCC 7942. J Biol Chem 269: 16143–16147

    Google Scholar 

  • vanDorssen RJ, Breton J, Plijter JJ, Satoh K, vanGorkom HJ and Amesz J (1987) Spectroscopic properties of the reaction center and of the 47 kDa chlorophyll protein of Photosystem II. Biochim Biophys Acta 893: 267–274

    Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M and Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of Photosystem II: Stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408–1412

    Google Scholar 

  • Vermass WFJ and Ikeuchi M (1991) Photosystem II. In: Bogorad L and Vasil IK (eds) The Photosynthetic Apparatus: Molecular Biology and Operation Cell Culture and Somatic Cell Genetics of Plants, Vol 7B, pp 25–111. Academic Press. San Diego

    Google Scholar 

  • Wünschmann G and Brand JJ (1992) Rapid turnover of a component required for photosynthesis explains temperature dependence and kinetics of phtoinhibition in a cyanobacterium, Synechococcus 6301. Planta 186: 426–433

    Google Scholar 

  • Zurawski G, Bohnert HJ, Whitfeld PR and Bottomley W (1982) Nucleotide sequence of the gene for the 32 000-Mr thylakoid membrane protein from Spinacia oleracea and Nicotiana debnevi predicts a totally conserved primary translation product of Mr 38 950. Proc Natl Acad Sci USA 79: 7699–7703

    Google Scholar 

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Authors and Affiliations

  1. Department of Plant Physiology, University of Umeå, S-901 87, Umeå, Sweden

    Gunnar Öquist, Douglas Campbell, Adrian K. Clarke & Petter Gustafsson

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  1. Gunnar Öquist
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  2. Douglas Campbell
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  3. Adrian K. Clarke
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  4. Petter Gustafsson
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Öquist, G., Campbell, D., Clarke, A.K. et al. The cyanobacterium Synechococcus modulates Photosystem II function in response to excitation stress through D1 exchange. Photosynth Res 46, 151–158 (1995). https://doi.org/10.1007/BF00020425

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  • DOI: https://doi.org/10.1007/BF00020425

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