Abstract
We have examined the molecular and photosynthetic responses of a planktonic cyanobacterium to shifts in light intensity over periods up to one generation (7 h). Synechococcus sp. PCC 7942 possesses two functionally distinct forms of the D1 protein, D1∶1 and D1∶2. Photosystem II (PSII) centers containing D1∶1 are less efficient and more susceptible to photoinhibition than are centers containing D 1∶2. Under 50 μmol photons· m−2·s−1, PSII centers contain D1∶1, but upon shifts to higher light (200 to 1000 μmol photons·m−2·s−1), D1∶1 is rapidly replaced by D 1∶2, with the rate of interchange dependent on the magnitude of the light shift. This interchange is readily reversed when cells are returned to 50 μmol photons·m−2·s−1. If, however, incubation under 200 μmol photons·m−2·s−1 is extended, D1∶1 content recovers and by 3 h after the light shift D1∶1 once again predominates. Oxygen evolution and chlorophyll (Chl) fluorescence measurements spanning the light shift and D1 interchanges showed an initial inhibition of photosynthesis at 200 μmol photons·m−2·s−1, which correlates with a proportional loss of total D1 protein and a cessation of growth. This was followed by recovery in photosynthesis and growth as the maximum level of D 1∶2 is reached after 2 h at 200 μmol photons·m−2·s−1. Thereafter, photosynthesis steadily declines with the loss of D1∶2 and the return of the less-efficient D1∶1. During the D1∶1/D1∶2 interchanges, no significant change occurs in the level of phycocyanin (PC) and Chl a, nor of the phycobilisome rod linkers. Nevertheless, the initial PC/Chl a ratio strongly influences the magnitude of photo inhibition and recovery during the light shifts. In Synechococcus sp. PCC 7942, the PC/Chl a ratio responds only slowly to light intensity or quality, while the rapid but transient interchange between D1∶1 and D 1∶2 modulates PSII activity to limit damage upon exposure to excess light.
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Abbreviations
- Chl:
-
chlorophyll
- F′M :
-
maximum Chl fluorescence in light-adapted state
- F′v :
-
variable Chl fluorescence in light-adapted state PC-phycocyanin
- PPFD:
-
photosynthetic photon flux density
- qp :
-
photochemical quenching
References
Bhalerao RP, Lind LK, Gustafsson P (1994) Cloning of the cpcE and cpcF genes from Synechococcus sp. PCC 6301 and their inactivation in Synechococcus sp. PCC 7942. Plant Mol Biol 26:313–326
Bouyoub A, Vernotte C, Astier C (1993) Functional analysis of the homologous psbA gene copies in Synechocystis PCC 6714 and PCC 6803. Plant Mol Biol 21:249–258
Bustos SA, 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
Bustos SA, Schaefer MR, Golden SS (1990) Different and rapid responses of four cyanobacterial psbA transcripts to changes in light intensity. J Bacteriol 172:1998–2004
Campbell D, Zhou G, Gustafsson P, Öquist G, Clarke AK (in press) Electron transport regulates exchange of two forms of photosystem II DI protein in the cyanobacterium Synechococcus. EMBO J
Chow WS, Osmond CB, Huang LK (1989) Photosystem function and herbicide binding sites during photoinhibition of spinach chloroplasts in vivo and in vitro. Photosynth Res 21:17–26
Clarke AK, Critchley C (1992) The identification of a heat shock protein complex in chloroplasts of barley leaves. Plant Physiol 100:2081–2089
Clarke, AK, Soitamo A, Gustafsson P, 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
Clarke AK, Hurry VM, Gustafsson P, 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
Curtis SE, 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
De Las Rivas J, Andersson B, 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
Eley JH (1971) Effect of carbon dioxide concentration of pigmentation in the blue-green algae Anacystis nidulans. Plant Cell Physiol 12:311–316
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Gingrich JC, Buzby JS, Stirewalt VL, 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
Golden SS, Brusslan J, 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
Golden SS, Cho D-SC, Nalty MS (1989) Two functional psbD genes in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171:4707–4713
Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) Environmental effects on the light-harvesting complex of cyanobacteria. J Bacteriol 175:575–582
Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39
Jansson C, Debus RJ, Osiewacz HD, Gurevitz M, McIntosh L (1987) Construction of an obligate photoheterotrophic mutant of the cyanobacterium Synechocystis 6803 Plant Physiol 85:1021–1025
Krupa Z, Öquist G, Gustafsson P (1990) Photoinhibition and recovery of photosynthesis in psbA gene-inactivated strains of cyanobacterium Anacystis nidulans. Plant Physiol 93:1–6
Krupa Z, Öquist G, 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
Kulkarni RD, 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
Lönneborg A, Kalla SR, Samuelsson G, Gustafsson P, Öquist G (1988) Light-regulated expression of the psbA transcript in the cyanobacterium Anacystis nidulans. FEBS Lett 240:110–114
Maxwell DP, Falk S, Trick CG, Huner NPA (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105:535–543
Manodori A, Melis A (1984) Photochemical apparatus organization in Anacystis nidulans (cyanobacteria). Effect of CO2 concentration during cell growth. Plant Physiol 74:67–71
Miller AG, Espie GS, Canvin DT (1991) The effects of inorganic carbon and oxygen on fluorescence in the cyanobacterium Synechococcus UTEX 625. Can J Bot 69:1151–1160
Muller C, Reuter W, Wehrmeyer W, Dau H, Senger H (1993) Adaptation of the photosynthetic apparatus of Anacystis nidulans to irradiance and CO2-concentration. Bot Acta 106:480–487
Mulligan B, Schultes N, Chen L, 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
Murata N, Fork D (1975) Temperature dependence of chlorophyll a fluorescence in relation to the physical phase of membrane lipids in algae and higher plants Plant Phys 56:791–796
Myers J, Graham JR, Wang RT (1980) Light harvesting in Anacystis nidulans studied in pigment mutants. Plant Physiol 66:1144–1149
Öquist G, Chow WS, Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186:450–460
Ottander C, Hundal T, Andersson B, Huner NPA, Öquist G (1993) Low temperature photoinhibition in barley results in structurally stable photosystem II reaction centers. Photosynth Res 35:191–200
Reuter W, Müller C (1993) Adaptation of the photosynthetic apparatus of cyanobacteria to light and CO2. J Photochem Photobiol B: Biol 21:3–27
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stainer RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Samuelsson G, Lönnesborg A, Rosenqvist E, Gustafsson P, Öquist G (1985) Photoinhibition and reactivation of photosynthesis in the cyanobacterium Anacystis nidulans Plant Physiol 79:992–995
Samuelsson G, Lönneborg A, Gustafsson P, 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
Schaefer MR, Golden SS (1989) Differential expression of members of a cyanobacterial psbA gene family in response to light. J Bacteriol 171:3973–3981
Shipton CA, Barber J (1991) Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: Evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci USA 88:6691–6695
Shyam R, Raghavendra AS, Sane PV (1993) Role of dark respiration in photoinhibition of photosynthesis and its reactivation in the cyanobacterium Anacystis nidulans. Physiol Plant 88:446–452
Soitamo AJ, Zhou G, Clarke AK, Öquist G, Aro E-M, Gustafsson P (1994) Over-production of the D1 protein of photosystem II reaction centre in the cyanobacterium Synechococcus sp. PCC 7942. Plant Mol Biol 26:709–721
Tandeau de Marsac N, Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: New steps towards molecular mechanisms. FEMS Microbiol. Rev 104:119–190
Tyystjärvi E, Kettunen R, Aro E-M. (1994) The rate constant of photoinhibition in vitro is independent of the antenna size of photosystem II but depends on temperature. Biochim Biophys Acta 1186:177–185
van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosyn Res 25:147–150
Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, 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
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The authors would like to thank Professor Eva-Mari Aro (Department of Biology, University of Turku, Finland) for her gift of the total D1 antibody, and Dr Vaughan M. Hurry (RSBS, Australian National University, Canberra, Australia) for his critical reading of the manuscript. This research was supported by the Swedish Natural Science Research Council.
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Clarke, A.K., Campbell, D., Gustafsson, P. et al. Dynamic responses of photosystem II and phycobilisomes to changing light in the cyanobacterium Synechococcus sp. PCC 7942. Planta 197, 553–562 (1995). https://doi.org/10.1007/BF00196678
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DOI: https://doi.org/10.1007/BF00196678