Abstract
Recent studies of responses of cyanobacterial cells to salt stress have revealed that the NaCl-induced decline in the photosynthetic activities of photosystems II and I involves rapid and slow changes. The rapid decreases in the activities of both photosystems, which occur within a few minutes, are reversible and are associated with osmotic effects, which induce the efflux of water from the cytosol through water channels and rapidly increase intracellular concentrations of salts. Slower decreases in activity, which occur within hours, are irreversible and are associated with ionic effects that are due to the influx of Na+ and Cl− ions through K+(Na+) channels and, probably, Cl− channels, with resultant dissociation of extrinsic proteins from photosystems. In combination with light stress, salt stress significantly stimulates photoinhibition by inhibiting repair of photodamaged photosystem II. Tolerance of photosystems to salt stress can be enhanced by genetically engineered increases in the unsaturation of fatty acids in membrane lipids and by intracellular synthesis of compatible solutes, such as glucosylglycerol and glycinebetaine. In this review, we summarize recent progress in research on the effects of salt stress on photosynthesis in cyanobacteria.
Similar content being viewed by others
Abbreviations
- BQ:
-
1,4-Benzoquinone
- CCCP:
-
Carbonyl cyanide m-chlorophenylhydrazone
- Chl:
-
Chlorophyll
- CSA:
-
p-Chloromercuriphenyl-sulfonic acid
- DCIP:
-
2,6-Dichlorophenolindophenol
- DCMU:
-
3-(3′,4′-Dichlorophenyl)-1,1-dimethylurea
- DPC:
-
Diphenylcarbazide
- FCCP:
-
Carbonyl cyanide p-trifluoro-methoxyphenylhydrazone
- GG:
-
Glucosylglycerol
- MV:
-
Methylviologen
- PSII:
-
Photosystem II
- PSI:
-
Photosystem I
- ROS:
-
Reactive oxygen species
References
Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition a historical perspective. Photosynth Res 76:343–370. doi:10.1023/A:1024969518145
Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32. doi:10.1016/j.bbabio.2004.03.003
Allakhverdiev SI, Nishiyama Y, Suzuki I, Tasaka Y, Murata N (1999) Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc Natl Acad Sci USA 96:5862–5867. doi:10.1073/pnas.96.10.5862
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Murata N (2000a) Inactivation of photosystems I and II in response to osmotic stress in Synechococcus: Contribution of water channels. Plant Physiol 122:1201–1208. doi:10.1104/pp.122.4.1201
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000b) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056. doi:10.1104/pp.123.3.1047
Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853. doi:10.1104/pp.125.4.1842
Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y et al (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443–1453. doi:10.1104/pp.011114
Allakhverdiev SI, Klimov VV, Hagemann M (2005) Cellular energization protects the photosynthetic machinery against salt-induced inactivation in Synechococcus. Biochim Biophys Acta 1708:201–208. doi:10.1016/j.bbabio.2005.01.002
Allakhverdiev SI, Deshnium P, Mohanty P, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta-Bioenergetics 1767:1363–1371
Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A (2007) A bacterial transgene for catalase protects translation of D1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol 145:258–265. doi:10.1104/pp.107.101733
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi:10.1016/0005-2728(93)90134-2
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396. doi:10.1104/pp.106.082040
Bhagwat AA, Apte SK (1989) Comparative analysis of proteins induced by heat shock, salinity, and osmotic stress in the nitrogen-fixing cyanobacterium Anabaena sp. strain L-31. J Bacteriol 171:5187–5189
Blumwald E, Wolosin JM, Packer L (1984) Na+/H+ exchange in the cyanobacterium Synechococcus 6311. Biochem Biophys Res Commun 22:452–459. doi:10.1016/0006-291X(84)90497-2
Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC et al (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311. doi:10.1016/S0981-9428(00)01237-7
Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. doi:10.1016/S1369-5266(02)00255-8
Demmig-Adams B, Adams WWIII (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626. doi:10.1146/annurev.pp.43.060192.003123
Demmig-Adams B, Adams WWIII (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153. doi:10.1126/science.1078002
Deshnium P, Los DA, Hayashi H, Mustardy L, Murata N (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–907. doi:10.1007/BF00014964
Ferjani A, Mustardy I, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637. doi:10.1104/pp.102.017277
Fulda S, Huckauf J, Schoor A, Hagemann M (1999) Analysis of stress responses in the cyanobacterial strains Synechococcus sp. PCC 7942, Synechocystis sp. PCC 6803, Synechococcus sp. PCC:7418 Osmolyte accumulation and stress protein synthesis. J Plant Physiol 154:240–249
Golbeck JH (1994) Photosystem I in cyanobacteria. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 319–360
Hagemann M, Erdmann N (1994) Activation and pathway of glucosylglycerol synthesis in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 140:1427–1431
Hagemann M, Erdmann N (1997) Environmental stresses. In: Rai AK (ed) Cyanobacterial Nitrogen Metabolism and Environmental Biotechnology. Springer-Verlag, Heidelberg, pp 156–221
Hagemann M, Wolfel L, Kruger B (1990) Alterations of protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 after a salt shock. J Gen Microbiol 136:1393–1399
Hagemann M, Techel D, Rensing L (1991) Comparison of salt- and heat-induced alterations of protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 155:587–592. doi:10.1007/BF00245354
Hagemann M, Schoor A, Jeanjean R, Zuther E, Joset F (1997) The stpA gene from Synechocystis sp. strain PCC 6803 encodes the glucosylglycerolphosphate phosphatase involved in cyanobacterial osmotic response to salt shock. J Bacteriol 179:1727–1733
Hayashi H, Murata N (1998) Genetically engineered enhancement of salt tolerance in higher plants. In: Sato K, Murata N (eds) Stress responses of photosynthetic organisms. Molecular mechanisms and molecular regulation. Elsevier, Amsterdam, pp 133–148
Hibino T, Lee BH, Rai AK, Ishikawa H, Kojima H, Tawada H et al (2000) Salt enhances photosystem I content and cyclic electron flow via NAD(P)H dehydrogenase in the halotolerant cyanobacterium Aphanothece halophytica. Aust J Plant Physiol 23:321–330
Huflejt ME, Tremolieres A, Pineau B, Lang JK, Hatheway J, Packer L (1990) Changes in membrane lipid composition during saline growth of the fresh water cyanobacterium Synechococcus 6311. Plant Physiol 94:1512–1521
Inaba M, Sakamoto A, Murata N (2001) Functional expression in Escherichia coli of low-affinity and high-affinity Na+(Li+)/H+ antiporters of Synechocystis. J Bacteriol 183:1376–1384. doi:10.1128/JB.183.4.1376-1384.2001
Izawa S (1980) Acceptors and donors for chloroplast electron transport. Methods Enzymol 69:413–435. doi:10.1016/S0076-6879(80)69041-7
Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738–744. doi:10.1111/j.1399-3054.1996.tb00251.x
Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136. doi:10.1093/dnares/3.3.109
Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290:339–348. doi:10.1006/bbrc.2001.6201
Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, Hayashi H et al (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol 65:936–947. doi:10.1111/j.1365-2958.2007.05836.x
Kuwabara T, Murata N (1983) Quantitative analysis of the inactivation of photosynthetic oxygen evolution and the release of polypeptides and manganese in the photosystem II particles of spinach chloroplasts. Plant Cell Physiol 24:741–747
Marin K, Stirnberg M, Eisenhut M, Kramer R, Hagemann M (2006) Osmotic stress in Synechocystis sp. PCC 6803: low tolerance towards nonionic osmotic stress results from lacking activation of glucosylglycerol accumulation. Microbiology 152:2023–2030. doi:10.1099/mic.0.28771-0
Miyao M, Murata N (1983) Partial disintegration and reconstitution of the photosynthetic oxygen-evolution system: binding of 24 kD and 18 kD polypeptides. Biochim Biophys Acta 725:87–93. doi:10.1016/0005-2728(83)90227-X
Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94:217–224. doi:10.1007/s11120-007-9184-y
Murata N, Miyao M (1985) Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends Biochem Sci 10:122–124. doi:10.1016/0968-0004(85)90272-5
Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713. doi:10.1038/356710a0
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421. doi:10.1016/j.bbabio.2006.11.019
Nakamura T, Yuda R, Unemoto T, Bakker EP (1998) KtrAB, a new type of bacterial K+ -uptake system from Vibrio alginolyticus. J Bacteriol 180:3491–3494
Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568. doi:10.1146/annurev.arplant.47.1.541
Nishiyama Y, Los DA, Hayashi H, Murata N (1997) Thermal protection of the oxygen-evolving machinery by PsbU, an extrinsic protein of photosystem II in Synechococcus sp PCC 7002. Plant Physiol 115:1473–1480. doi:10.1104/pp.115.4.1473
Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus sp PCC 7002. Plant Physiol 120:301–308. doi:10.1104/pp.120.1.301
Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7. doi:10.1007/s11120-004-6434-0
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. doi:10.1016/j.bbabio.2006.05.013
Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of the D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiol 141:758–765. doi:10.1104/pp.106.076976
Öquist G, Campbell D, Clarke A, Gustafsson P (1995) The cyanobacterium Synechococcus modulates photosystem II function in response to excitation stress through D1 exchange. Photosynth Res 46:151–158. doi:10.1007/BF00020425
Paithoonrangsarid K, Shoumskaya MA, Kanesaki Y, Satoh S, Tabata S, Los DA et al (2004) Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem 279:53078–53086. doi:10.1074/jbc.M410162200
Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44:243–252. doi:10.1007/BF00048597
Pfenning N (1978) General physiology and ecology of photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 3–18
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44. doi:10.1146/annurev.pp.35.060184.000311
Reed RH, Stewart WDP (1988) The responses of cyanobacteria to salt stress. In: Rogers LJ, Gallan LJ (eds) Biochemistry of the algae and cyanobacteria, vol 12. Clarendon Press, Oxford, pp 217–231
Reed RH, Warr SRC, Richardson DL, Moore DJ, Stewart WDP (1985) Multiphasic osmotic adjustment in a euryhaline cyanobacterium. FEMS Microbiol Lett 28:225–229. doi:10.1111/j.1574-6968.1985.tb00796.x
Sakurai I, Hagio M, Gombos Z, Tyystjarvi T, Paakkarinen V, Aro E-M et al (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol 133:376–1384. doi:10.1104/pp.103.026955
Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H (2007) Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol 144:1336–1346. doi:10.1104/pp.107.098731
Shapiguzov A, Lyukevich AA, Allakhverdiev SI, Sergeyenko TV, Suzuki I, Murata N et al (2005) Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates the osmostress-inducible gene expression. Microbiology 151:447–455. doi:10.1099/mic.0.27530-0
Shen J-R, Ikeuchi M, Inoue Y (1992) Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus. FEBS Lett 301:145–149. doi:10.1016/0014-5793(92)81235-E
Shen J-R, Qian M, Inoue Y, Burnap RL (1998) Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37:1551–1558. doi:10.1021/bi971676i
Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M et al (2005) Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J Biol Chem 280:21531–21538. doi:10.1074/jbc.M412174200
Suno R, Niwa H, Tsuchiya D, Zhang X, Yoshida M, Morikawa K (2006) Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol Cell 22:575–585. doi:10.1016/j.molcel.2006.04.020
Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi:10.1016/j.tplants.2008.01.005
Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K et al (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416–6425
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. doi:10.1016/S0076-6879(80)69067-3
Wada H, Murata N (1989) Synechocystis PCC 6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978
Wada H, Gombos Z, Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347:200–203. doi:10.1038/347200a0
Yamashita T, Butler WL (1969) Inhibition of the Hill reaction by Tris and restoration by electron donation to photosystem II. Plant Physiol 44:435–438
Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant.53.091401.143329
Acknowledgments
This work was supported, in part, by the Cooperative Research Program on Stress-Tolerant Plants of the National Institute for Basic Biology, Japan, and by grants from the Russian Foundation for Basic Research (Nos. 08-04-00241 and 08-04-91300) and from the Molecular and Cell Biology Programs of the Russian Academy of Sciences (to S.I.A.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Allakhverdiev, S.I., Murata, N. Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98, 529–539 (2008). https://doi.org/10.1007/s11120-008-9334-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-008-9334-x