Skip to main content

Advertisement

Log in

Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses

  • Current Topics in Plant Research
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Photosynthetic organisms have evolved various acclimatory responses to high-light (HL) conditions to maintain a balance between energy supply (light harvesting and electron transport) and consumption (cellular metabolism) and to protect the photosynthetic apparatus from photodamage. The molecular mechanism of HL acclimation has been extensively studied in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Whole genome DNA microarray analyses have revealed that the change in gene expression profile under HL is closely correlated with subsequent acclimatory responses such as (1) acceleration in the rate of photosystem II turnover, (2) downregulation of light harvesting capacity, (3) development of a protection mechanism for the photosystems against excess light energy, (4) upregulation of general protection mechanism components, and (5) regulation of carbon and nitrogen assimilation. In this review article, we survey recent progress in the understanding of the molecular mechanisms of these acclimatory responses in Synechocystis sp. PCC 6803. We also briefly describe attempts to understand HL acclimation in various cyanobacterial species in their natural environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adamska I (2001) The Elip family of stress proteins in the thylakoid membrane of pro- and eukaryota. In: Aro EM, Andersson B (eds) Advances in photosynthesis and respiration—regulation of photosynthesis, vol 11. Kluwer Academic Publishers, Dordrecht, pp 487–505

    Google Scholar 

  • Alfonso M, Perewoska I, Constant S, Kirilovsky D (1999) Redox control of psbA expression in cyanobacterium Synechocystis strains. J Photochem Photobiol B Biol 48:104–113

    Article  CAS  Google Scholar 

  • Alfonso M, Perewoska I, Kirilovsky D (2000) Redox control of psbA gene expression in the cyanobacterium Synechocystis PCC 6803. Involvement of the cytochrome b 6/f complex. Plant Physiol 122:505–516

    Article  PubMed  CAS  Google Scholar 

  • Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro EM (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem 286:24007–24014

    Article  PubMed  CAS  Google Scholar 

  • Anderson LE (1971) Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases. Biochim Biophys Acta 235:237–244

    PubMed  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  PubMed  CAS  Google Scholar 

  • Asadulghani SuzukiY, Nakamoto H (2003) Light plays a key role in the modulation of heat shock response in the cyanobacterium Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 306:872–879

    Article  PubMed  CAS  Google Scholar 

  • Ashby MK, Houmard J (2006) Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Microbiol Mol Biol Rev 70:472–509

    Article  PubMed  CAS  Google Scholar 

  • Ashby MK, Mullineaux CW (1999) Cyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMS Microbiol Lett 181:253–260

    Article  PubMed  CAS  Google Scholar 

  • Baena-Gonzalez E, Baginsky S, Mulo P, Summer H, Aro EM, Link G (2001) Chloroplast transcription at different light intensities. Glutathione-mediated phosphorylation of the major RNA polymerase involved in redox-regulated organellar gene expression. Plant Physiol 127:1044–1052

    Article  PubMed  CAS  Google Scholar 

  • Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem Photobiol 84:1410–1420

    Article  PubMed  CAS  Google Scholar 

  • Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277:2006–2011

    Article  PubMed  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  PubMed  CAS  Google Scholar 

  • Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The Deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347–30355

    Article  PubMed  CAS  Google Scholar 

  • Battchikova N, Vainonen JP, Vorontsova N, Keranen M, Carmel D, Aro EM (2010) Dynamic changes in the proteome of Synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J Proteome Res 9:5896–5912

    Article  PubMed  CAS  Google Scholar 

  • Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336

    Article  PubMed  CAS  Google Scholar 

  • Bernroitner M, Zamocky M, Furtmüller PG, Peschek GA, Obinger C (2009) Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria. J Exp Bot 60:423–440

    Article  PubMed  CAS  Google Scholar 

  • Bhaya D, Dufresne A, Vaulot D, Grossman A (2002) Analysis of the hli gene family in marine and freshwater cyanobacteria. FEMS Microbiol Lett 215:209–219

    Article  PubMed  CAS  Google Scholar 

  • Bissati K, Kirilovsky D (2001) Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol 125:1988–2000

    Article  PubMed  Google Scholar 

  • Bissati K, Delphin E, Murata N, Etienne A, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457:229–242

    Article  PubMed  Google Scholar 

  • Boulay C, Abasova L, Six C, Vass I, Kirilovsky D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta 1777:1344–1354

    Article  PubMed  CAS  Google Scholar 

  • Boulay C, Wilson A, D’Haene S, Kirilovsky D (2010) Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci USA 107:11620–11625

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683

    PubMed  CAS  Google Scholar 

  • Clausen T, Southan C, Ehrmann M (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10:443–455

    Article  PubMed  CAS  Google Scholar 

  • Collier JL, Grossman AR (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047

    PubMed  CAS  Google Scholar 

  • Douce R, Bourguignon J, Neuburger M, Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6:167–176

    Article  PubMed  CAS  Google Scholar 

  • Driever SM, Baker NR (2011) The water–water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO2 assimilation is restricted. Plant Cell Environ 34:837–846

    Article  PubMed  CAS  Google Scholar 

  • Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci USA 105:17199–17204

    Article  PubMed  CAS  Google Scholar 

  • Eriksson J, Salih GF, Ghebramedhin H, Jansson C (2000) Deletion mutagenesis of the 5’ psbA2 region in Synechocystis 6803: identification of a putative cis element involved in photoregulation. Mol Cell Biol Res Commun 3:292–298

    Article  PubMed  CAS  Google Scholar 

  • Fernández-González B, Martínez-Férez IM, Vioque A (1998) Characterization of two carotenoid gene promoters in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1443:343–351

    PubMed  Google Scholar 

  • Forchhammer K (2010) The network of P(II) signalling protein interactions in unicellular cyanobacteria. Adv Exp Med Biol 675:71–90

    Article  PubMed  CAS  Google Scholar 

  • Fujimori T, Higuchi M, Sato H, Aiba H, Muramatsu M, Hihara Y, Sonoike K (2005a) The mutant of sll1961, which encodes a putative transcriptional regulator, has a defect in regulation of photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 139:408–416

    Article  PubMed  CAS  Google Scholar 

  • Fujimori T, Hihara Y, Sonoike K (2005b) PsaK2 subunit in photosystem I is involved in state transition under high light condition in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 280:22191–22197

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Murakami A, Aizawa K, Ohki K (1994) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 677–692

    Google Scholar 

  • Fukuda SY, Yamakawa R, Hirai M, Kashino Y, Koike H, Satoh K (2008) Mechanisms to avoid photoinhibition in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol 49:488–492

    Article  PubMed  CAS  Google Scholar 

  • Fulda S, Huang F, Nilsson F, Hagemann M, Norling B (2000) Proteomics of Synechocystis sp. strain PCC 6803. Identification of periplasmic proteins in cells grown at low and high salt concentrations. Eur J Biochem 267:5900–5907

    Article  PubMed  CAS  Google Scholar 

  • Gaber A, Tamoi M, Takeda T, Nakano Y, Shigeoka S (2001) NADPH-dependent glutathione peroxidase-like proteins (Gpx-1, Gpx-2) reduce unsaturated fatty acid hydroperoxides in Synechocystis PCC 6803. FEBS Lett 499:32–36

    Article  PubMed  CAS  Google Scholar 

  • Gaber A, Yoshimura K, Tamoi M, Takeda T, Nakano Y, Shigeoka S (2004) Induction and functional analysis of two reduced nicotinamide adenine dinucleotide phosphate-dependent glutathione peroxidase-like proteins in Synechocystis PCC 6803 during the progression of oxidative stress. Plant Physiol 136:2855–2861

    Article  PubMed  CAS  Google Scholar 

  • García-Domínguez M, Reyes JC, Florencio FJ (2000) NtcA represses transcription of gifA and gifB, genes that encode inhibitors of glutamine synthetase type I from Synechocystis sp. PCC 6803. Mol Microbiol 35:1192–1201

    Article  PubMed  Google Scholar 

  • Gilles-Gonzalez MA, Gonzalez G (2004) Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol 96:774–783

    Article  PubMed  CAS  Google Scholar 

  • Golden SS (1994) Light-responsive gene expression and the biochemistry of the photosystem II reaction center. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 693–714

    Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749

    PubMed  CAS  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    Article  PubMed  CAS  Google Scholar 

  • Hackenberg C, Engelhardt A, Matthijs HC, Wittink F, Bauwe H, Kaplan A, Hagemann M (2009) Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp. strain PCC 6803. Planta 230:625–637

    Article  PubMed  CAS  Google Scholar 

  • Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta 1706:68–80

    Article  PubMed  CAS  Google Scholar 

  • Hanaoka M, Tanaka K (2008) Dynamics of RpaB-promoter interaction during high light stress, revealed by chromatin immunoprecipitation (ChIP) analysis in Synechococcus elongatus PCC 7942. Plant J 56:327–335

    Article  PubMed  CAS  Google Scholar 

  • Harel Y, Ohad I, Kaplan A (2004) Activation of photosynthesis and resistance to photoinhibition in cyanobacteria within biological desert crust. Plant Physiol 136:3070–3079

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Guedeney G, He Q, Grossman AR (2003) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim Biophys Acta 1557:21–33

    Article  PubMed  CAS  Google Scholar 

  • He Q, Dolganov N, Bjorkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314

    Article  PubMed  CAS  Google Scholar 

  • Heddad M, Adamska I (2002) The evolution of light stress proteins in photosynthetic organisms. Comp Funct Genomics 3:504–510

    Article  PubMed  CAS  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  PubMed  CAS  Google Scholar 

  • Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A (2005) Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol 138:2292–2298

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Prieto MA, Tibiletti T, Abasova L, Kirilovsky D, Vass I, Funk C (2011) The small CAB-like proteins of the cyanobacterium Synechocystis sp. PCC 6803: their involvement in chlorophyll biogenesis for Photosystem II. Biochim Biophys Acta 1807:1143–1151

    Article  PubMed  CAS  Google Scholar 

  • Herranen M, Aro EM, Tyystjärvi T (2001) Two distinct mechanisms regulate the transcription of photosystem II genes in Synechocystis sp. PCC 6803. Physiol Plant 112:531–539

    Article  PubMed  CAS  Google Scholar 

  • Hihara Y (1999) The molecular mechanism for acclimation to high light in cyanobacteria. Curr Top Plant Biol 1:37–50

    CAS  Google Scholar 

  • Hihara Y, Ikeuchi M (1997) Mutation in a novel gene required for photomixotrophic growth leads to enhanced photoautotrophic growth of Synechocystis sp. PCC 6803. Photosynth Res 53:243–252

    Article  CAS  Google Scholar 

  • Hihara Y, Sonoike K, 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 117:1205–1216

    Article  PubMed  CAS  Google Scholar 

  • Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806

    Article  PubMed  CAS  Google Scholar 

  • Hihara Y, Sonoike K, Kanehisa M, Ikeuchi M (2003) DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:1719–1725

    Article  PubMed  CAS  Google Scholar 

  • Hishiya S, Hatakeyama W, Mizota Y, Hosoya-Matsuda N, Motohashi K, Ikeuchi M, Hisabori T (2008) Binary reducing equivalent pathways using NADPH-thioredoxin reductase and ferredoxin-thioredoxin reductase in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol 49:11–18

    Article  PubMed  CAS  Google Scholar 

  • Horiuchi M, Nakamura K, Kojima K, Nishiyama Y, Hatakeyama W, Hisabori T, Hihara Y (2010) The PedR transcriptional regulator interacts with thioredoxin to connect photosynthesis with gene expression in cyanobacteria. Biochem J 431:135–140

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Hosoya-Matsuda N, Motohashi K, Yoshimura H, Nozaki A, Inoue K, Ohmori M, Hisabori T (2005) Anti-oxidative stress system in cyanobacteria. Significance of type II peroxiredoxin and the role of 1-Cys peroxiredoxin in Synechocystis sp. strain PCC 6803. J Biol Chem 280:840–846

    PubMed  CAS  Google Scholar 

  • Hsiao HY, He Q, Van Waasbergen LG, Grossman AR (2004) Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J Bacteriol 186:3882–3888

    Article  PubMed  CAS  Google Scholar 

  • Huang L, McCluskey MP, Ni H, LaRossa RA (2002) Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol 184:6845–6858

    Article  PubMed  CAS  Google Scholar 

  • Huang F, Hedman E, Funk C, Kieselbach T, Schröder WP, Norling B (2004) Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol Cell Proteomics 3:586–595

    Article  PubMed  CAS  Google Scholar 

  • Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910–920

    Article  PubMed  CAS  Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2009) Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Res Microbiol 160:726–732

    Article  PubMed  CAS  Google Scholar 

  • Imamura S, Asayama M, Takahashi H, Tanaka K, Takahashi H, Shirai M (2003a) Antagonistic dark/light-induced SigB/SigD, group 2 sigma factors, expression through redox potential and their roles in cyanobacteria. FEBS Lett 554:357–362

    Article  PubMed  CAS  Google Scholar 

  • Imamura S, Yoshihara S, Nakano S, Shiozaki N, Yamada A, Tanaka K, Takahashi H, Asayama M, Shirai M (2003b) Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium. J Mol Biol 325:857–872

    Article  PubMed  CAS  Google Scholar 

  • Ishii A, Hihara Y (2008) An AbrB-like transcriptional regulator, Sll0822, is essential for the activation of nitrogen-regulated genes in Synechocystis sp. PCC 6803. Plant Physiol 148:660–670

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231

    Article  PubMed  CAS  Google Scholar 

  • Jansén T, Kidron H, Taipaleenmäki H, Salminen T, Mäenpää P (2005) Transcriptional profiles and structural models of the Synechocystis sp. PCC 6803 Deg proteases. Photosynth Res 84:57–63

    Article  PubMed  CAS  Google Scholar 

  • Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119

    Article  PubMed  CAS  Google Scholar 

  • Kada S, Koike H, Satoh K, Hase T, Fujita Y (2003) Arrest of chlorophyll synthesis and differential decrease of Photosystems I and II in a cyanobacterial mutant lacking light-independent protochlorophyllide reductase. Plant Mol Biol 51:225–235

    Article  PubMed  CAS  Google Scholar 

  • 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, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, 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 3:109–136

    Article  PubMed  CAS  Google Scholar 

  • Kanervo E, Spetea C, Nishiyama Y, Murata N, Andersson B, Aro EM (2003) Dissecting a cyanobacterial proteolytic system: efficiency in inducing degradation of the D1 protein of photosystem II in cyanobacteria and plants. Biochim Biophys Acta 1607:131–140

    Article  PubMed  CAS  Google Scholar 

  • Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N (2007) Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J 49:313–324

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Hagemann M, Bauwe H, Kahlon S, Ogawa T (2008) Carbon acquisition by cyanobacteria: mechanisms, comparative genomics and evolution. In: Herrero A, Flores E (eds) The cyanobacteria: molecular biology, genomics and evolution, Caister Academic Press, Norfork, pp 305–334

  • Kappell AD, van Waasbergen LG (2007) The response regulator RpaB binds the high light regulatory 1 sequence upstream of the high-light-inducible hliB gene from the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 187:337–342

    Article  PubMed  CAS  Google Scholar 

  • Kappell AD, Bhaya D, van Waasbergen LG (2006) Negative control of the high light-inducible hliA gene and implications for the activities of the NblS sensor kinase in the cyanobacterium Synechococcus elongatus strain PCC 7942. Arch Microbiol 186:403–413

    Article  PubMed  CAS  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    Article  PubMed  CAS  Google Scholar 

  • Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004–8012

    Article  PubMed  CAS  Google Scholar 

  • Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int Rev Cell Mol Biol 280:185–218

    Article  PubMed  CAS  Google Scholar 

  • Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S, Chen F, Lapidus A, Ferriera S, Johnson J, Steglich C, Church GM, Richardson P, Chisholm SW (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3:e231

    Article  PubMed  CAS  Google Scholar 

  • Kettunen R, Pursiheimo S, Rintamaki E, Van Wijk KJ, Aro EM (1997) Transcriptional and translational adjustments of psbA gene expression in mature chloroplasts during photoinhibition and subsequent repair of photosystem II. Eur J Biochem 247:441–448

    Article  PubMed  CAS  Google Scholar 

  • Kilian O, Steunou AS, Fazeli F, Bailey S, Bhaya D, Grossman AR (2007) Responses of a thermophilic Synechococcus isolate from the microbial mat of Octopus Spring to light. Appl Environ Microbiol 73:4268–4278

    Article  PubMed  CAS  Google Scholar 

  • Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16

    Article  PubMed  CAS  Google Scholar 

  • Klughammer B, Baier M, Dietz K-J (1998) Inactivation by gene disruption of 2-cysteine-peroxidation in Synechocystis sp. PCC 6803 leads to increased stress sensitivity. Physiol Plant 104:699–706

    Article  CAS  Google Scholar 

  • Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB, Ikeuchi M (2004) Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 45:290–299

    Article  PubMed  CAS  Google Scholar 

  • Kojima K, Nakamoto H (2007) A novel light- and heat-responsive regulation of the groE transcription in the absence of HrcA or CIRCE in cyanobacteria. FEBS Lett 581:1871–1880

    Article  PubMed  CAS  Google Scholar 

  • Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, Hayashi H, Nishiyama Y (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol 65:936–947

    Article  PubMed  CAS  Google Scholar 

  • Komenda J (2000) Role of two forms of the D1 protein in the recovery from photoinhibition of photosystem II in the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1457:243–252

    Article  PubMed  CAS  Google Scholar 

  • Komenda J, Barker M, Kuviková S, de Vries R, Mullineaux CW, Tichy M, Nixon PJ (2006) The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp. PCC 6803. J Biol Chem 281:1145–1151

    Article  PubMed  CAS  Google Scholar 

  • Komura M, Yamagishi A, Shibata Y, Iwasaki I, Itoh S (2010) Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy. Biochim Biophys Acta 1797:331–338

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564

    Article  PubMed  CAS  Google Scholar 

  • Krzywda S, Brzozowski AM, Verma C, Karata K, Ogura T, Wilkinson AJ (2002) The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 angstrom resolution. Structure 10:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Kufryk G, Hernandez-Prieto MA, Kieselbach T, Miranda H, Vermaas W, Funk C (2008) Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II. Photosynth Res 95:135–145

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278

    Article  PubMed  CAS  Google Scholar 

  • Lieman-Hurwitz J, Haimovich M, Shalev-Malul G, Ishii A, Hihara Y, Gaathon A, Lebendiker M, Kaplan A (2009) A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression. Environ Microbiol 11:927–936

    Article  PubMed  CAS  Google Scholar 

  • López-Redondo ML, Moronta F, Salinas P, Espinosa J, Cantos R, Dixon R, Marina A, Contreras A (2010) Environmental control of phosphorylation pathways in a branched two-component system. Mol Microbiol 78:475–489

    Article  PubMed  CAS  Google Scholar 

  • Maeda H, Sakuragi Y, Bryant DA, Dellapenna D (2005) Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol 138:1422–1435

    Article  PubMed  CAS  Google Scholar 

  • Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C (2000) Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 479:72–77

    Article  PubMed  CAS  Google Scholar 

  • Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100:9061–9066

    Article  PubMed  CAS  Google Scholar 

  • Mary I, Tu CJ, Grossman A, Vaulot D (2004) Effects of high light on transcripts of stress-associated genes for the cyanobacteria Synechocystis sp. PCC 6803 and Prochlorococcus MED4 and MIT9313. Microbiology 150:1271–1281

    Article  PubMed  CAS  Google Scholar 

  • Mehler AH (1951) Studies on reactivities of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77

    Article  PubMed  CAS  Google Scholar 

  • Midorikawa T, Matsumoto K, Narikawa R, Ikeuchi M (2009) An Rrf2-type transcriptional regulator is required for expression of psaAB genes in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 151:882–892

    Article  PubMed  CAS  Google Scholar 

  • Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Microbiol 46:905–915

    Article  PubMed  CAS  Google Scholar 

  • Min KT, Hilditch CM, Diederich B, Errington J, Yudkin MD (1993) Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. Cell 74:735–742

    Article  PubMed  CAS  Google Scholar 

  • Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008) Identification of two homologous genes, chlAI and chlAII, that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283:2684–2692

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Montesinos ML, Muro-Pastor AM, Herrero A, Flores E (1998) Ammonium/methylammonium permeases of a cyanobacterium. Identification and analysis of three nitrogen-regulated amt genes in Synechocystis sp. PCC 6803. J Biol Chem 273:31463–31470

    Article  PubMed  CAS  Google Scholar 

  • Mooney RA, Darst SA, Landick R (2005) Sigma and RNA polymerase: an on-again, off-again relationship? Mol Cell 20:335–345

    Article  PubMed  CAS  Google Scholar 

  • Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710

    Article  PubMed  CAS  Google Scholar 

  • Murakami A, Fujita Y (1991) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC 6714 in response to light-intensity. Plant Cell Physiol 32:223–230

    CAS  Google Scholar 

  • Muramatsu M, Hihara Y (2003) Transcriptional regulation of genes encoding subunits of photosystem I during acclimation to high-light conditions in Synechocystis sp. PCC 6803. Planta 216:446–453

    PubMed  CAS  Google Scholar 

  • Muramatsu M, Hihara Y (2006) Characterization of high-light-responsive promoters of the psaAB genes in Synechocystis sp. PCC 6803. Plant Cell Physiol 47:878–890

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu M, Hihara Y (2007) Coordinated high-light response of genes encoding subunits of photosystem I is achieved by AT-rich upstream sequences in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 189:2750–2758

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu M, Sonoike K, Hihara Y (2009) Mechanism of downregulation of photosystem I content under high-light conditions in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 155:989–996

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235–247

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  PubMed  CAS  Google Scholar 

  • Nakamura K, Hihara Y (2006) Photon flux density-dependent gene expression in Synechocystis sp. PCC 6803 is regulated by a small, redox-responsive, LuxR-type regulator. J Biol Chem 281:36758–36766

    Article  PubMed  CAS  Google Scholar 

  • Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8

    Article  PubMed  CAS  Google Scholar 

  • Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S, Omata T (2008) Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Mol Microbiol 68:98–109

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  PubMed  CAS  Google Scholar 

  • Niwa H, Tsuchiya D, Makyio H, Yoshida M, Morikawa K (2002) Hexameric ring structure of the ATPase domain of the membrane-integrated metalloprotease FtsH from Thermus thermophilus HB8. Structure 10:1415–1423

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A (2010) Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One 5:e11000

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  PubMed  CAS  Google Scholar 

  • Omata T (1995) Structure, function and regulation of the nitrate transport system of the cyanobacterium Synechococcus sp. PCC7942. Plant Cell Physiol 36:207–213

    PubMed  CAS  Google Scholar 

  • Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96:13571–13576

    Article  PubMed  CAS  Google Scholar 

  • Osanai T, Tanaka K (2007) Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. Plant Cell Physiol 48:908–914

    Article  PubMed  CAS  Google Scholar 

  • Osanai T, Ikeuchi M, Tanaka K (2008) Group 2 sigma factors in cyanobacteria. Physiol Plant 133:490–506

    Article  PubMed  CAS  Google Scholar 

  • Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127

    PubMed  CAS  Google Scholar 

  • Passardi F, Zamocky M, Favet J, Jakopitsch C, Penel C, Obinger C, Dunand C (2007) Phylogenetic distribution of catalase-peroxidases: are there patches of order in chaos? Gene 397:101–113

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Pérez ME, Mata-Cabana A, Sánchez-Riego AM, Lindahl M, Florencio FJ (2009) A comprehensive analysis of the peroxiredoxin reduction system in the Cyanobacterium Synechocystis sp. strain PCC 6803 reveals that all five peroxiredoxins are thioredoxin dependent. J Bacteriol 191:7477–7489

    Article  PubMed  CAS  Google Scholar 

  • Peter E, Wallner T, Wilde A, Grimm B (2011) Comparative functional analysis of two hypothetical chloroplast open reading frames (ycf) involved in chlorophyll biosynthesis from Synechocystis sp. PCC6803 and plants. J Plant Physiol 168:1380–1386

    Article  PubMed  CAS  Google Scholar 

  • Pojidaeva E, Zinchenko V, Shestakov SV, Sokolenko A (2004) Involvement of the SppA1 peptidase in acclimation to saturating light intensities in Synechocystis sp. strain PCC 6803. J Bacteriol 186:3991–3999

    Article  PubMed  CAS  Google Scholar 

  • Pollari M, Gunnelius L, Tuominen I, Ruotsalainen V, Tyystjärvi E, Salminen T, Tyystjärvi T (2008) Characterization of single and double inactivation strains reveals new physiological roles for group 2 sigma factors in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 147:1994–2005

    Article  PubMed  CAS  Google Scholar 

  • Pollari M, Ruotsalainen V, Rantamäki S, Tyystjärvi E, Tyystjärvi T (2009) Simultaneous inactivation of sigma factors B and D interferes with light acclimation of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 191:3992–4001

    Article  PubMed  CAS  Google Scholar 

  • Pollari M, Rantamäki S, Huokko T, Kårlund-Marttila A, Virjamo V, Tyystjärvi E, Tyystjärvi T (2011) Effects of deficiency and overdose of group 2 sigma factors in triple inactivation strains of Synechocystis sp. strain PCC 6803. J Bacteriol 193:265–273

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228–18233

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461

    Article  PubMed  CAS  Google Scholar 

  • Promnares K, Komenda J, Bumba L, Nebesarova J, Vacha F, Tichy M (2006) Cyanobacterial small chlorophyll-binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits. J Biol Chem 281:32705–32713

    Article  PubMed  CAS  Google Scholar 

  • Punginelli C, Wilson A, Routaboul JM, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the orange carotenoid protein. Biochim Biophys Acta 1787:280–288

    Article  PubMed  CAS  Google Scholar 

  • Rakhimberdieva MG, Stadnichuk IN, Elanskaya IV, Karapetyan NV (2004) Carotenoid-induced quenching of the phycobilisome fluorescence in photosystem II-deficient mutant of Synechocystis sp. FEBS Lett 574:85–88

    Article  PubMed  CAS  Google Scholar 

  • Ruch S, Beyer P, Ernst H, Al-Babili S (2005) Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol Microbiol 55:1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Rupprecht E, Düppre E, Schneider D (2010) Similarities and singularities of three DnaK proteins from the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 51:1210–1218

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto W (2003) Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana. Genes Genet Syst 78:1–9

    Article  PubMed  CAS  Google Scholar 

  • Sakayori T, Shiraiwa Y, Suzuki I (2009) A synechocystis homolog of SipA protein, Ssl3451, enhances the activity of the histidine kinase Hik33. Plant Cell Physiol 50:1439–1448

    Article  PubMed  CAS  Google Scholar 

  • Salinas P, Ruiz D, Cantos R, Lopez-Redondo ML, Marina A, Contreras A (2007) The regulatory factor SipA provides a link between NblS and NblR signal transduction pathways in the cyanobacterium Synechococcus sp. PCC 7942. Mol Microbiol 66:1607–1619

    PubMed  CAS  Google Scholar 

  • Sato H, Fujimori T, Sonoike K (2008) sll1961 is a novel regulator of phycobilisome degradation during nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 582:1093–1096

    Article  PubMed  CAS  Google Scholar 

  • Satoh K, Hirai M, Nishio J, Yamaji T, Kashino Y, Koike H (2002) Recovery of photosynthetic systems during rewetting is quite rapid in a terrestrial cyanobacterium, Nostoc commune. Plant Cell Physiol 43:170–176

    Article  PubMed  CAS  Google Scholar 

  • Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73:249–299

    Article  PubMed  CAS  Google Scholar 

  • Schäfer L, Vioque A, Sandmann G (2005) Functional in situ evaluation of photosynthesis-protecting carotenoids in mutants of the cyanobacterium Synechocystis PCC 6803. J Photochem Photobiol B 78:195–201

    Article  PubMed  CAS  Google Scholar 

  • Seino Y, Takahashi T, Hihara Y (2009) The response regulator RpaB binds to the upstream element of photosystem I genes to work for positive regulation under low-light conditions in Synechocystis sp. Strain PCC 6803. J Bacteriol 191:1581–1586

    Article  PubMed  CAS  Google Scholar 

  • Seki A, Hanaoka M, Akimoto Y, Masuda S, Iwasaki H, Tanaka K (2007) Induction of a group 2 sigma factor, RPOD3, by high light and the underlying mechanism in Synechococcus elongatus PCC 7942. J Biol Chem 282:36887–36894

    Article  PubMed  CAS  Google Scholar 

  • Sendersky E, Lahmi R, Shaltiel J, Perelman A, Schwarz R (2005) NblC, a novel component required for pigment degradation during starvation in Synechococcus PCC 7942. Mol Microbiol 58:659–668

    Article  PubMed  CAS  Google Scholar 

  • Shapira M, Lers A, Heifetz PB, Irihimovitz V, Osmond CB, Gillham NW, Boynton JE (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Mol Biol 33:1001–1011

    Article  PubMed  CAS  Google Scholar 

  • Shen G, Boussiba S, Vermaas WF (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98:11789–11794

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277:18658–18664

    Article  PubMed  CAS  Google Scholar 

  • Sicora CI, Ho FM, Salminen T, Styring S, Aro EM (2009) Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. Biochim Biophys Acta 1787:105–112

    Article  PubMed  CAS  Google Scholar 

  • Silva P, Choi YJ, Hassan HA, Nixon PJ (2002) Involvement of the HtrA family of proteases in the protection of the cyanobacterium Synechocystis PCC 6803 from light stress and in the repair of photosystem II. Philos Trans R Soc Lond B Biol Sci 357:1461–1467

    Article  PubMed  CAS  Google Scholar 

  • Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15:2152–2164

    Article  PubMed  CAS  Google Scholar 

  • Singh AK, Elvitigala T, Bhattacharyya-Pakrasi M, Aurora R, Ghosh B, Pakrasi HB (2008) Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the cyanobacterium Synechocystis. Plant Physiol 148:467–478

    Article  PubMed  CAS  Google Scholar 

  • Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann RG, Shestakov SV (2002) The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Curr Genet 41:291–310

    Article  PubMed  CAS  Google Scholar 

  • Sonoike K, Hihara Y, Ikeuchi M (2001) Physiological significance of the regulation of photosystem stoichiometry upon high light acclimation of Synechocystis sp. PCC 6803. Plant Cell Physiol 42:379–384

    Article  PubMed  CAS  Google Scholar 

  • Sozer O, Komenda J, Ughy B, Domonkos I, Laczkó-Dobos H, Malec P, Gombos Z, Kis M (2010) Involvement of carotenoids in the synthesis and assembly of protein subunits of photosynthetic reaction centers of Synechocystis sp. PCC 6803. Plant Cell Physiol 51:823–835

    Article  PubMed  CAS  Google Scholar 

  • Steglich C, Futschik M, Rector T, Steen R, Chisholm SW (2006) Genome-wide analysis of light sensing in Prochlorococcus. J Bacteriol 188:7796–7806

    Article  PubMed  CAS  Google Scholar 

  • Steunou AS, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E, Peters JW, Kühl M, Grossman AR (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103:2398–2403

    Article  PubMed  CAS  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    Article  PubMed  CAS  Google Scholar 

  • Stork T, Michel KP, Pistorius EK, Dietz KJ (2005) Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot 56:3193–3206

    Article  PubMed  CAS  Google Scholar 

  • Summerfield TC, Sherman LA (2007) Role of sigma factors in controlling global gene expression in light/dark transitions in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 189:7829–7840

    Article  PubMed  CAS  Google Scholar 

  • Summerfield TC, Toepel J, Sherman LA (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47:12939–12941

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19:1347–1361

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR, Murata N (2005) The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol 138:1409–1421

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Yamaguchi O, Omata T (2004) Roles of CmpR, a LysR family transcriptional regulator, in acclimation of the cyanobacterium Synechococcus sp. strain PCC 7942 to low-CO2 and high-light conditions. Mol Microbiol 52:837–845

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Nakai N, Muramatsu M, Hihara Y (2010) Role of multiple HLR1 sequences in the regulation of the dual promoters of the psaAB genes in Synechocystis sp. PCC 6803. J Bacteriol 192:4031–4036

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K (2011) Chloroplast transcriptional machinery of red algae: conservation of four types of transcriptional regulators in non-green chloroplasts. In: Mikami K (ed) Porphyra yezoensis. Nova Science Publishers, New york (in press)

  • Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L, Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganisms. Curr Biol 7:723–728

    Article  PubMed  CAS  Google Scholar 

  • Tchernov D, Silverman J, Luz B, Reinhold L, Kaplan A (2003) Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings. Photosynth Res 77:95–103

    Article  PubMed  CAS  Google Scholar 

  • Tichy M, Vermaas W (1999) In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. J Bacteriol 181:1875–1882

    PubMed  CAS  Google Scholar 

  • Tolbert NE (1997) The C-2 oxidative photosynthetic carbon cycle. Annu Rev Plant Physiol Plant Mol Biol 48:1–23

    Article  PubMed  CAS  Google Scholar 

  • Trebst A (1980) Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. Methods Enzymol 69:675–715

    Article  CAS  Google Scholar 

  • Tu CJ, Shrager J, Burnap RL, Postier BL, Grossman AR (2004) Consequences of a deletion in dspA on transcript accumulation in Synechocystis sp. strain PCC6803. J Bacteriol 186:3889–3902

    Article  PubMed  CAS  Google Scholar 

  • Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218

    Article  PubMed  Google Scholar 

  • Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall’Osto L, Carriere F, Bassi R, Grimm B, Nussaume L, Havaux M (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50:795–809

    Article  PubMed  CAS  Google Scholar 

  • Valladares A, Montesinos ML, Herrero A, Flores E (2002) An ABC-type, high-affinity urea permease identified in cyanobacteria. Mol Microbiol 43:703–715

    Article  PubMed  CAS  Google Scholar 

  • van Waasbergen LG, Dolganov N, Grossman AR (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184:2481–2490

    Article  PubMed  CAS  Google Scholar 

  • Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14:200–205

    Article  PubMed  CAS  Google Scholar 

  • Vavilin DV, Vermaas WF (2002) Regulation of the tetrapyrrole biosynthetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiol Plant 115:9–24

    Article  PubMed  CAS  Google Scholar 

  • Vavilin D, Yao D, Vermaas W (2007) Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803: kinetic analysis of pigment labeling with 15N and 13C. J Biol Chem 282:37660–37668

    Article  PubMed  CAS  Google Scholar 

  • Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87

    Article  PubMed  CAS  Google Scholar 

  • Vicente JB, Justino MC, Gonçalves VL, Saraiva LM, Teixeira M (2008) Biochemical, spectroscopic, and thermodynamic properties of flavodiiron proteins. Methods Enzymol 437:21–45

    Article  PubMed  CAS  Google Scholar 

  • Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279:5739–5751

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Jantaro S, Lu B, Majeed W, Bailey M, He Q (2008) The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147:1239–1250

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul JM, Kerfeld CA, van Grondelle R, Robert B, Kennis JT, Kirilovsky D (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci USA 105:12075–12080

    Article  PubMed  CAS  Google Scholar 

  • Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355:1517–1529

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Vavilin D, Funk C, Vermaas W (2002) Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 49:149–160

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Vavilin D, Funk C, Vermaas W (2004) Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803: consequences for pigment biosynthesis and accumulation. J Biol Chem 279:27971–27979

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Bernát G, Singh A, Mi H, Rögner M, Pakrasi HB, Ogawa T (2008) Properties of mutants of Synechocystis sp. strain PCC 6803 lacking inorganic carbon sequestration systems. Plant Cell Physiol 49:1672–1677

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Miyake C, Dietz KJ, Tomizawa K, Murata N, Yokota A (1999) Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 447:269–273

    Article  PubMed  CAS  Google Scholar 

  • Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MA, Tichy M, Vermaas W, Funk C (2007) Localization of the small CAB-like proteins in photosystem II. J Biol Chem 282:267–276

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura T, Imamura S, Tanaka K, Shirai M, Asayama M (2007) Cooperation of group 2 sigma factors, SigD and SigE for light-induced transcription in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 581:1495–1500

    Article  PubMed  CAS  Google Scholar 

  • Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J 37:864–876

    Article  PubMed  CAS  Google Scholar 

  • Zaltsman A, Ori N, Adam Z (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17:2782–2790

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS One 4:e5331

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Aaron Kaplan, Prof. Kintake Sonoike, Prof. Yoshitaka Nishiyama, and Mr. Takanori Nagano for critical reading of the manuscript and helpful suggestions. This work was supported by JST PRESTO program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yukako Hihara.

Additional information

Y. Hihara is the recipient of the BSJ Award for Young Scientist, 2009.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 44 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muramatsu, M., Hihara, Y. Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses. J Plant Res 125, 11–39 (2012). https://doi.org/10.1007/s10265-011-0454-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-011-0454-6

Keywords

Navigation