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UV-B induced differential transcription of psbD genes encoding the D2 protein of Photosystem II in the cyanobacterium Synechocystis 6803

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Abstract

UV-B irradiation of intact Synechocystis sp. PCC 6803 cells results in the loss of Photosystem II activity, which can be repaired via de novo synthesis of the D1 and D2 reaction center subunits. A key step in the repair process is the differential transcription of the psbA2 and psbA3 genes, coding for identical D1 polypeptides [Máté et al. (1998) J Biol Chem 273: 17439–17444]. In the present work, we investigated for the first time the effect of UV-B irradiation on the transcription of the psbD1 and psbD2 genes encoding identical D2 polypeptides. By using gene-specific S1 nuclease protection assay we showed differential UV-B induced transcription of the two psbD genes: the level of psbD1 mRNA was increased 1.5–2 fold, whereas the accumulation of psbD2 mRNA was 5–7 fold. The induction of psbD2 transcript accumulation by low intensity light was specific for the UV-B range. UV-A emission from the applied UV source, as well as 100 μE m−2 s−1 white light had negligible effect. Increase in the psbD2 mRNA level was observed at very low UV-B intensities, which did not cause damage to the function and protein structure of PS II. Expression patterns of chimeric genes containing the promoter regions of the psbD1, psbD2 genes fused to the firefly luciferase (luc) reporter gene showed similar induction as observed for the endogenous psbD genes. Our findings demonstrate that UV-B radiation induces differential expression of the of the psbD1 and psbD2 genes. We propose that the primarily expressed psbD2 serves as a UV stress gene and participates in a rapid defense response against UV-B stress. This effect is regulated, at least partially, at the level of transcription.

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References

  • Andersson B and Styring S (1991) Photosystem II: Molecular organization, function and acclimation. Curr Top Bioenerg 16: 1–81

    CAS  Google Scholar 

  • Bornman JF (1989) Target sites of UV-B radiation in photosynthesis of higher plants. J Photochem Photobiol B4: 145–158

    Google Scholar 

  • Brandle JR, Campbell WF, Sisson WB and Caldwell MM (1977) Net photosynthesis, electron transport capacity and ultrastucture of Pisum sativum L. exposed to ultraviolet-B radiation. Plant Physiol 60: 165–169

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Campbell D, Erikson M-J, Öquist G, Gustafsson P and Clarke AK (1998) The cyanobacteriumSynechochoccus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci USA 95: 364–369

    Article  PubMed  CAS  Google Scholar 

  • Chisholm D and Williams JGK (1988) Nucleotide sequence of psbC, the gene encoding the CP43 chlorophyll a-binding protein of Photosystem II, in the cyanobacterium Synechocystis 6803. Plant Mol Biol 10: 293–301

    Article  CAS  Google Scholar 

  • CyanoBase website (1996). http://zearth.kazusa.or.jp/cyano

  • Fejes E, Páy A, Kanevsky I, Széll M, Adám É, Kay S and Nagy F (1990) A 268 bp upstream sequence mediates the circadian clock regulated transcription of the wheat Cab-1 gene in transgenic plants. Plant Mol Biol 15: 921–932

    Article  PubMed  CAS  Google Scholar 

  • Friso G, Barbato R, Giacometti GM, and Barber J (1994) Degradation of D2 protein due to UV-B irradiation in the reaction centre of Photosystem II. FEBS Lett 339: 217–221

    Article  PubMed  CAS  Google Scholar 

  • Friso G, Spetea C, Giacometti GM, Vass I, and Barbato R (1993) Degradation of Photosystem II reaction center D1-protein induced by UVB irradiation in isolated thylakoids. Identification and characterization of C-and N-terminal breakdown products. Biochim Biophys Acta 1184: 78–84

    Google Scholar 

  • Golden SS (1995) Light-responsive gene expression in cyanobacteria. J Bacteriol 177: 1651–1654

    PubMed  CAS  Google Scholar 

  • Golden SS and Stearns GW (1988) Nucleotide sequence and transcript analysis of three Photosystem II genes from the cyanobacterium Synechococcus sp. PCC 7942. Gene 67: 85–96

    Article  PubMed  CAS  Google Scholar 

  • Green R and Fluhr R (1995) UV-B induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203–212

    Article  PubMed  CAS  Google Scholar 

  • Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK and Edelman M (1989) Separate photosensitizers mediate degradation of the 32-kDa Photosystem II reaction centre protein in visible and UV spectral regions. Proc Natl Acad Sci USA 86: 6617–6620

    Article  PubMed  CAS  Google Scholar 

  • Hideg E and Vass I (1996) UV-B induced free radical production in plant leaves and isolated thylakoid membranes. Plant Sci 115: 251–260

    Article  CAS  Google Scholar 

  • Hideg É, Kálai T, Hideg K and Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37: 11405–11411

    Article  PubMed  CAS  Google Scholar 

  • Jansen MAK, Gaba V and Greenberg BM (1998) Higher plants and UV-B radiation: Balancing damage, repair and acclimation. Trends Plant Sci 3: 131–135

    Article  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM, Mattoo AK and Edelman M (1996) Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of Photosystem-II. Plant J 9: 693–699

    Article  CAS  Google Scholar 

  • Kasting JF (1993) Earth's early atmosphere. Science 259: 920–926

    PubMed  CAS  Google Scholar 

  • Kerr JB and McElroy CT (1993) Evidence for upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262: 1032–1034

    CAS  PubMed  Google Scholar 

  • Kulandaivelu G and Noorudeen AM (1983) Comparative study on the action of ultraviolet-C and utraviolet-B radiation on photosynthetic electron transport. Physiol Plant 58: 389–394

    Article  CAS  Google Scholar 

  • Máté Z, Sass L, Szekeres M, Vass I and Nagy F (1998) UV-B induced differential transcription of psbA genes encoding the D1 protein of Photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273: 17439–17444

    Article  PubMed  Google Scholar 

  • Melis A, Nemson JA and Harrison MA (1992) Damage to functional components and partial degradation of Photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. Biochim Biophys Acta 1100: 312–320

    CAS  Google Scholar 

  • Mohamed A and Jansson C (1989) Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13: 693–700

    Article  PubMed  CAS  Google Scholar 

  • Mohamed A and Jansson C (1991) Photosynthetic electron transport controls degradation but not production of psbA transcripts in the cyanobacterium Synechocystis 6803. PlantMol Biol 16: 891–897

    Article  CAS  Google Scholar 

  • Mohamed A, Eriksson J, Osiewacz HD and Jansson C (1993) Differential expression of the psbA genes in the cyanobacterium Synechocystis 6803. Mol Gen Genet 238: 161–168

    PubMed  CAS  Google Scholar 

  • Nagy F, Kay SA and Chua N-H (1988) Analysis of gene expression in transgenic plants. In: Gelvin SB and Schilperoort RA (eds) Plant Molecular Biology Manual, pp 1–29. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Nogués S and Baker NR (1995) Evaluation of the role of damage to photosystem II in the inhibition of CO2 assimilation in pea leaves on exposure to UV-B radiation. Plant Cell Environ 18: 781–787

    Article  Google Scholar 

  • Rontó GY, Fekete A, Gáspár S and Módos K (1989) Action spectra for photoinduced inactivation of bacteriophage T7 sensitized by 8-methoxypsoralen and angelicin. J Photochem Photobiol 3B: 497–507

    Google Scholar 

  • Salih GF and Jansson C (1997) Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp. strain 6803 produces a novel and functional D1 protein. Plant Cell 9: 869–878

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF and Maniatis T (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sass L, Spetea C, Máté Z, Nagy F and Vass I (1997) Repair of UVB induced damage of Photosystem II via de novo synthesis of the D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth Res 54: 55–62

    Article  CAS  Google Scholar 

  • Smith RC, Prézelin BB, Baker KS, Bidigare RR, Boucher NP, Coley T, Karentz D, MacIntyre S, Matlick HA, Menzies D, Ondrusek M, Wan Z and Waters KJ (1995) Ozone depletion: Ultraviolet radiation and phytoplankton biology in antarctic waters. Science 255: 952–959

    Google Scholar 

  • Strid A, Chow WS and Anderson JM (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum Sativum. Biochim Biophys Acta 1020: 260–268

    Article  CAS  Google Scholar 

  • Svensson B, Vass I and Styring S (1991) Comparison of the amino acid sequence of the D1 and D2 reaction center proteins in Photosystem II from different organisms. Z Naturforsch 46C: 765–776

    Google Scholar 

  • Trebst A and Depka B (1990) Degradation of the D-1 protein subunit of Photosystem II in isolated thylakoids by UV light. Z Naturforsch 45c: 765–771

    Google Scholar 

  • Tyystjärvi T, Tyystjärvi E, Ohad I and Aro E-M (1998) Exposure of Synechocystis 6803 cells to series of single turnover flashes increases the psbA transcript level by activating transcription and down-regulating psbA mRNA degradation. FEBS Lett 436: 483–487

    Article  PubMed  Google Scholar 

  • Tyystjärvi T, Mulo P, Mäenpää P and Aro EM (1996) D1 polypeptide degradation may regulate psbA gene expression at transcriptional and translational levels in Synechocystis sp PCC 6803. Photosynth Res 47: 111–120

    Article  Google Scholar 

  • Vass I (1996) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of Photosynthesis, pp 931–950. Marcel Dekker, New York

    Google Scholar 

  • Williams GK (1988) Construction of specific mutations in Photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766–778

    Article  CAS  Google Scholar 

  • Williams JGK and Chisholm DA (1986) Nucleotide sequences of both psbD genes from the cyanobacterium Synechocystis 6803. In: Biggins J (ed) Progress in Photosynthesis Research, pp 809–812. Martinus Nijhoff, Dordrecht, The Netherlands

    Google Scholar 

  • Yu J and Vermaas WFJ (1990) Transcript levels and synthesis of Photosystem II components in cyanobacterial mutants with inactivated Photosystem II genes. Plant Cell 2: 315–322

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Hu X, Henkow L, Jordan BR, and Strid A (1994) The effects of ultraviolet-B radiation on the CF0F1-ATPase. Biochim Biophys Acta 1185: 295–302

    Article  CAS  Google Scholar 

Download references

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Correspondence to Imre Vass.

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Viczián, A., Máté, Z., Nagy, F. et al. UV-B induced differential transcription of psbD genes encoding the D2 protein of Photosystem II in the cyanobacterium Synechocystis 6803. Photosynthesis Research 64, 257–266 (2000). https://doi.org/10.1023/A:1006444932137

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