Abstract
When photosynthetic organisms are exposed to abiotic stress, their photosynthetic activity is significantly depressed. In particular, photosystem II (PSII) in the photosynthetic machinery is readily inactivated under strong light and this phenomenon is referred to as photoinhibition of PSII. Other types of abiotic stress act synergistically with light stress to accelerate photoinhibition. Recent studies of photoinhibition have revealed that light stress damages PSII directly, whereas other abiotic stresses act exclusively to inhibit the repair of PSII after light-induced damage (photodamage). Such inhibition of repair is associated with suppression, by reactive oxygen species (ROS), of the synthesis of proteins de novo and, in particular, of the D1 protein, and also with the reduced efficiency of repair under stress conditions. Gene-technological improvements in the tolerance of photosynthetic organisms to various abiotic stresses have been achieved via protection of the repair system from ROS and, also, by enhancing the efficiency of repair via facilitation of the turnover of the D1 protein in PSII. In this review, we summarize the current status of research on photoinhibition as it relates to the effects of abiotic stress and we discuss successful strategies that enhance the activity of the repair machinery. In addition, we propose several potential methods for activating the repair system by gene-technological methods.
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References
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, 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, Murata N (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, Mohanty P, Murata N (2003) Dissection of photodamage at low temperature and repair in darkness suggests the existence of an intermediate form of photodamaged photosystem II. Biochemistry 42:14277–14283. doi:10.1021/bi035205
Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137:263–273. doi:10.1104/pp. 104.054478
Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371. doi:10.1016/j.bbabio.2007.10.005
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
Anderson JM, Chow WS (2002) Structural and functional dynamics of plant photosystem II. Philos Trans R Soc Lond B Biol Sci 357:1421–1430. doi:10.1098/rstb.2002.1138
Aono M, Saji H, Sakamoto A, Tanaka K, Kondo N, Tanaka K (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase. Plant Cell Physiol 36:1687–1691
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134
Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356. doi:10.1093/jxb/eri041
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi:10.1146/annurev.arplant.50.1.601
Asada K, Badger MR (1984) Photoreduction of 18O2 and H2 18O with concomitant evolution of 16O2 in intact spinach chloroplasts: evidence for scavenging of hydrogen peroxide by peroxidase. Plant Cell Physiol 25:1169–1179
Barrs HD (1971) Cyclic variations in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. Annu Rev Plant Physiol 22:223–236
Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol Plant Mol Biol 31:491–543. doi:10.1146/annurev.pp.31.060180.002423
Bersanini L, Battchikova N, Jokel M, Rehman A, Vass I, Allahverdiyeva Y, Aro EM (2014) Flavodiiron protein Flv2/Flv4-related photoprotective mechanism dissipates excitation pressure of PSII in cooperation with phycobilisomes in cyanobacteria. Plant Physiol 164:805–818. doi:10.1104/pp. 113.231969
Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci U S A 93:6320–6325
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
Chen THH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505. doi:10.1016/j.tplants.2008.06.007
Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20. doi:10.1111/J.1365-3040.2010.02232.X
Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci U S A 97:13430–13435. doi:10.1073/pnas.230451497
Delfine S, Alvino A, Zacchini M, Loreto F (1998) Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves. Aust J Plant Physiol 25:395–402
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
Deshnium P, Gombos Z, Nishiyama Y, Murata N (1997) The action in vivo of glycine betaine in enhancement of tolerance of Synechococcus sp. strain PCC 7942 to low temperature. J Bacteriol 179:339–344
Di Mascio P, Devasagayam TPA, Kaiser S, Sies H (1990) Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers. Biochem Soc Trans 18:1054–1056
Eckardt NA, Portis AR Jr (1997) Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol 113:243–248
Ejima K, Kawaharada T, Inoue S, Kojima K, Nishiyama Y (2012) A change in the sensitivity of elongation factor G to oxidation protects photosystem II from photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett 586:778–783. doi:10.1016/j.febslet.2012.01.042
Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H, Katoh S (1994) Is the primary cause of thermal inactivation of oxygen evolution in spinach PSII membranes release of the extrinsic 33 kDa protein or of Mn? Biochim Biophys Acta 1186:52–58. doi:10.1016/0005-2728(94)90134-1
Eriksson MJ, Clarke AK (1996) The heat shock protein ClpB mediates the development of thermotolerance in the cyanobacterium Synechococcus sp strain PCC 7942. J Bacteriol 178:4839–4846
Feller U, Crafts-Brandner SJ, Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116:539–546. doi:10.1104/pp. 116.2.539
Fork DC, Sen A, Williams WP (1987) The relationship between heat-stress and photobleaching in green and blue-green algae. Photosynth Res 11:71–87. doi:10.1007/Bf00117675
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100. doi:10.1104/pp. 110.166181
Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109:1047–1057. doi:10.1104/pp. 109.3.1047
Fukuzawa H, Ogawa T, Kaplan A (2012) The uptake of CO2 by cyanobacteria and microalgae. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds), Photosynthesis: plastid biology, energy conversion and carbon assimilation, advances in photosynthesis and respiration, Springer, Dordrecht, 34:625–650
Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 6:2733–2745. doi:10.1002/pmic.200500538
Gold L (1988) Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 57:199–233. doi:10.1146/annurev.bi.57.070188.001215
Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proc Natl Acad Sci U S A 91:8787–8791
Gombos Z, Kanervo E, Tsvetkova N, Sakamoto T, Aro EM, Murata N (1997) Genetic enhancement of the ability to tolerate photoinhibition by introduction of unsaturated bonds into membrane glycerolipids. Plant Physiol 115:551–559
Greer DH, Berry JA, Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168:253–260
Grennan AK, Ort DR (2007) Cool temperatures interfere with D1 synthesis in tomato by causing ribosomal pausing. Photosynth Res 94:375–385. doi:10.1007/s11120-007-9169-x
Guo SJ, Zhou HY, Zhang XS, Li XG, Meng QW (2007) Overexpression of CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J Plant Physiol 164:126–136. doi:10.1016/j.jplph.2006.01.004
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. doi:10.1016/j.bbabio.2004.09.001
Hakkila K, Antal T, Rehman AU, Kurkela J, Wada H, Vass I, Tyystjärvi E, Tyystjärvi T (2014) Oxidative stress and photoinhibition can be separated in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1837:217–225. doi:10.1016/j.bbabio.2013.11.011
Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167:176–183. doi:10.1016/J.Jplph.2009.08.009
Havaux M (1992) Stress tolerance of photosystem II in vivo—antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiol 100:424–432. doi:10.1104/pp. 100.1.424
Havaux M, Eymery F, Porfirova S, Rey P, Dormann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469. doi:10.1105/tpc.105.037036
Hideg E, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1186:143–152
Hideg E, Kos PB, Vass I (2007) Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol Plant 131:33–40. doi:10.1111/j.1399-3054.2007.00913.x
Holmström KO, Somersalo S, Mandal A, Palva TE, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51:177–185
Hossain MM, Nakamoto H (2002) HtpG plays a role in cold acclimation in cyanobacteria. Curr Microbiol 44:291–296. doi:10.1007/s00284-001-0005-9
Hossain MM, Nakamoto H (2003) Role for the cyanobacterial HtpG in protection from oxidative stress. Curr Microbiol 46:70–76. doi:10.1007/s00284-002-3831-5
Inoue S, Ejima K, Iwai E, Hayashi H, Appel J, Tyystjärvi E, Murata N, Nishiyama Y (2011) Protection by α-tocopherol of the repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1807:236–241. doi:10.1016/j.bbabio.2010.11.003
Jimbo H, Noda A, Hayashi H, Nagano T, Yumoto I, Orikasa Y, Okuyama H, Nishiyama Y (2013) Expression of a highly active catalase VktA in the cyanobacterium Synechococcus elongatus PCC 7942 alleviates the photoinhibition of photosystem II. Photosynth Res 117:509–515. doi:10.1007/s11120-013-9804-7
Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41:1037–1043
Kanervo E, Tasaka Y, Murata N, Aro EM (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures. Plant Physiol 114:841–849. doi:10.1104/pp.114.3.841
Kanesaki Y, Los DA, Suzuki I, Murata N (2010) Sensors and signal transducers of environmental stress in cyanobacteria. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological molecular and genomic foundation. Springer, Dordrecht, pp 15–31
Kaplan A (1981) Photoinhibition in Spirulina platensis—response of photosynthesis and HCO3 − uptake capability to CO2- depleted conditions. J Exp Bot 32:669–677. doi:10.1093/jxb/32.4.669
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. Horizon Scientific, Norwich, pp 305–334
Katano Y, Nimura-Matsune K, Yoshikawa H (2006) Involvement of DnaK3, one of the three DnaK proteins of cyanobacterium Synechococcus sp. PCC7942, in translational process on the surface of the thylakoid membrane. Biosci Biotechnol Biochem 70:1592–1598
Keren N, Berg A, van Kan PJ, Levanon H, Ohad I (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci U S A 94:1579–1584
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. doi:10.1111/j.1365-2958.2007.05836.x
Kojima K, Motohashi K, Morota T, Oshita M, Hisabori T, Hayashi H, Nishiyama Y (2009) Regulation of translation by the redox state of elongation factor G in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 284:18685–18691. doi:10.1074/jbc.M109.015131
Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21:234–244
Kornyeyev D, Logan BA, Payton P, Allen RD, Holaday AS (2001) Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpressing genes encoding chloroplast-targeted antioxidant enzymes. Physiol Plant 113:323–331. doi:10.1034/J.1399-3054.2001.1130304.X
Kornyeyev D, Logan BA, Allen RD, Holaday AS (2003) Effect of chloroplastic overproduction of ascorbate peroxidase on photosynthesis and photoprotection in cotton leaves subjected to low temperature photoinhibition. Plant Sci 165:1033–1041. doi:10.1016/S0168-9452(03)00294-2
Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564. doi:10.1007/s11120-008-9349-3
Kuroda H, Inagaki N, Satoh K (1992) The level of stromal ATP regulates translation of the D1 protein in isolated chloroplasts. Plant Cell Physiol 33:33–39
Kuroda H, Kobayashi K, Kaseyama H, Satoh K (1996) Possible involvement of a low redox potential component(s) downstream of photosystem I in the translational regulation of the D1 subunit of the photosystem II reaction center in isolated pea chloroplasts. Plant Cell Physiol 37:754–761
Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 120:173–181. doi:10.1104/pp. 120.1.173
Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673. doi:10.1111/J.1467-7652.2011.00611.X
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Li XP, Müller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci U S A 99:15222–15227. doi:10.1073/pnas.232447699
Li M, Ji L, Yang X, Meng Q, Guo S (2012a) The protective mechanisms of CaHSP26 in transgenic tobacco to alleviate photoinhibition of PSII during chilling stress. Plant Cell Rep 31:1969–1979. doi:10.1007/s00299-012-1309-x
Li ZR, Keasling JD, Niyogi KK (2012b) Overlapping photoprotective function of vitamin E and carotenoids in Chlamydomonas. Plant Physiol 158:313–323. doi:10.1104/pp. 111.181230
Lidholm J, Gustafsson P, Öquist G (1987) Photoinhibition of photosynthesis and its recovery in the green alga Chlamydomonas reinhardii. Plant Cell Physiol 28:1133–1140
Lintala M, Lehtimaki N, Benz JP, Jungfer A, Soll J, Aro EM, Bolter B, Mulo P (2012) Depletion of leaf-type ferredoxin-NADP+ oxidoreductase results in the permanent induction of photoprotective mechanisms in Arabidopsis chloroplasts. Plant J 70:809–817. doi:10.1111/j.1365-313X.2012.04930.x
Logan BA, Monteiro G, Kornyeyev D, Payton P, Allen RD, Holaday AS (2003) Transgenic overproduction of glutathione reductase does not protect cotton, Gossypium hirsutum (Malvaceae), from photoinhibition during growth under chilling conditions. Am J Bot 90:1400–1403. doi:10.3732/ajb.90.9.1400
Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photoprotection. Photosynth Res 88:119–132. doi:10.1007/s11120-006-9043-2
Los DA, Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394:3–15. doi:10.1016/S0005-2760(98)00091-5
Los DA, Suzuki I, Zinchenko VV, Murata N (2007) Stress responses in Synechocystis: regulated genes and regulatory systems. In: Herrero A, Flores E (eds) Cyanobacteria: molecular biology, genomics and evolution caister. Caister Academic Press, pp 117–157
Lu C-M, Zhang J-H (1999) Effects of salt stress on PSII function and photoinhibition in the cyanobacterium Spirulina platensis. J Plant Physiol 155:740–745
Mamedov M, Hayashi H, Murata N (1993) Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron-transport and phosphorylation reactions in Synechocystis PCC6803. Biochim Biophys Acta 1142:1–5. doi:10.1016/0005-2728(93)90077-S
Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51:190–200. doi:10.1093/pcp/pcp177
Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci U S A 81:1380–1384
Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135. doi:10.1016/S1360-1385(99)01387-4
Miller AG, Canvin DT (1989) Glycoaldehyde inhibits CO2 fixation in the cyanobacterium Synechococcus UTEX 625 without inhibiting the accumulation of inorganic carbon or the associated quenching of chlorophyll a fluorescence. Plant Physiol 91:1044–1049. doi:10.1104/pp. 91.3.1044
Miyagawa Y, Tamoi M, Shigeoka S (2000) Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol 41:311–320
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
Moon BY, Higashi S, Gombos Z, Murata N (1995) Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc Natl Acad Sci U S A 92:6219–6223
Mota-Cadenas C, Alcaraz-Lopez C, Martinez-Ballesta MC, Carvajal M (2010) How salinity affects CO2 fixation by horticultural crops. HortSci 45:1798–1803
Mulo P, Sirpiö S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98:489–501. doi:10.1007/s11120-008-9320-3
Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1–8
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
Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133. doi:10.1016/j.bbabio.2012.02.020
Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953. doi:10.1111/J.1365-313x.2004.02092.X
Nagano T, Kojima K, Hisabori T, Hayashi H, Morita EH, Kanamori T, Miyagi T, Ueda T, Nishiyama Y (2012) Elongation factor G is a critical target during oxidative damage to the translation system of Escherichia coli. J Biol Chem 287:28697–28704. doi:10.1074/jbc.M112.378067
Nakamoto H, Suzuki N, Roy SK (2000) Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection to the photosynthetic apparatus in cyanobacteria. FEBS Lett 483:169–174
Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 807:127–133. doi:10.1016/0005-2728(85)90115-X
Neale PJ, Melis A (1989) Salinity-stress enhances photoinhibition of photosystem II in Chlamydomonas reinhardtii. J Plant Physiol 134:619–622
Neely WC, Martin JM, Barker SA (1988) Products and relative reaction rates of the oxidation of tocopherols with singlet molecular oxygen. Photochem Photobiol 48:423–428
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, Kovács E, Lee CB, Hayashi H, Watanabe T, Murata N (1993) Photosynthetic adaptation to high temperature associated with thylakoid membranes of Synechococcus PCC7002. Plant Cell Physiol 34:337–343
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. doi:10.1093/emboj/20.20.5587
Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330. doi:10.1021/bi036178q
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
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. doi:10.1111/j.1399-3054.2011.01457.x
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. doi:10.1093/jxb/eri021
Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382. doi:10.1093/jxb/eri056
Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol Plant Mol Biol 35:415–442. doi:10.1146/annurev.pp.35.060184.002215
Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp PCC 7942. Plant Physiol 141:758–765. doi:10.1104/pp. 106.076976
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. doi:10.1021/bi047518q
Öquist G, Huner NPA (1991) Effects of cold-acclimation on the susceptibility of photosynthesis to photoinhibition in scots pine and in winter and spring cereals—a fluorescence analysis. Funct Ecol 5:91–100. doi:10.2307/2389559
Öquist G, Hurry VM, Huner NPA (1993) Low-temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol 101:245–250
Osmond CB (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98
Osmond CB (1997) C-4 photosynthesis: thirty or forty years on. Aust J Plant Physiol 24:409–412
Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362
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
Payton P, Webb R, Kornyeyev D, Allen R, Holaday AS (2001) Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J Exp Bot 52:2345–2354. doi:10.1093/jexbot/52.365.2345
Plaut Z, Bachmann E, Oertli JJ (1991) The effect of salinity on light and dark CO2 fixation of salt-adapted and unadapted cell cultures of Atriplex and tomato. J Exp Bot 42:531–535. doi:10.1093/Jxb/42.4.531
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44
Price GD (2011) Inorganic carbon transporters of the cyanobacterial CO2-concentrating mechanism. Photosynth Res 109:47–57. doi:10.1007/s11120-010-9608-y
Radmer RJ, Kok B (1976) Photoreduction of O2 primes and replaces CO2 assimilation. Plant Physiol 58:336–340. doi:10.1104/Pp.58.3.336
Radmer R, Ollinger O (1980) Light-driven uptake of oxygen, carbon dioxide, and bicarbonate by the green alga Scenedesmus. Plant Physiol 65:723–729. doi:10.1104/pp. 65.4.723
Rehman AU, Cser K, Sass L, Vass I (2013) Characterization of singlet oxygen production and its involvement in photodamage of photosystem II in the cyanobacterium Synechocystis PCC 6803 by histidine-mediated chemical trapping. Biochim Biophys Acta 1827:689–698. doi:10.1016/j.bbabio.2013.02.016
Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384. doi:10.1146/annurev.arplant.44.1.357
Rodriguez RE, Lodeyro A, Poli HO, Zurbriggen M, Peisker M, Palatnik JF, Tognetti VB, Tschiersch H, Hajirezaei MR, Valle EM, Carrillo N (2007) Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress. Plant Physiol 143:639–649. doi:10.1104/pp. 106.090449
Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88
Sakamoto A, Murata N (2001) The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol 125:180–188
Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171
Sakthivel K, Watanabe T, Nakamoto H (2009) A small heat-shock protein confers stress tolerance and stabilizes thylakoid membrane proteins in cyanobacteria under oxidative stress. Arch Microbiol 191:319–328. doi:10.1007/s00203-009-0457-z
Samuelsson G, Lonneborg 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, Lonneborg 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. doi:10.1104/pp.83.2.438
Sarvikas P, Hakala M, Pätsikkä E, Tyystjärvi T, Tyystjärvi E (2006) Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol 47:391–400. doi:10.1093/pcp/pcj006
Sarvikas P, Tyystjärvi T, Tyystjärvi E (2010) Kinetics of prolonged photoinhibition revisited: photoinhibited photosystem II centres do not protect the active ones against loss of oxygen evolution. Photosynth Res 103:7–17. doi:10.1007/s11120-009-9496-1
Schroda M, Vallon O, Wollman FA, Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11:1165–1178
Schuster G, Even D, Kloppstech K, Ohad I (1988) Evidence for protection by heat-shock proteins against photoinhibition during heat shock. EMBO J 7:1–6
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319. doi:10.1093/jexbot/53.372.1305
Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217. doi:10.1146/annurev.arplant.58.091406.110525
Shikanai T, Takeda T, Yamauchi H, Sano S, Tomizawa KI, Yokota A, Shigeoka S (1998) Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts. FEBS Lett 428:47–51. doi:10.1016/S0014-5793(98)00483-9
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
Sirikhachornkit A, Shin JW, Baroli I, Niyogi KK (2009) Replacement of alpha-tocopherol by beta-tocopherol enhances resistance to photooxidative stress in a xanthophyll-deficient strain of Chlamydomonas reinhardtii. Eukaryot Cell 8:1648–1657. doi:10.1128/ec.00124-09
Slabas AR, Suzuki I, Murata N, Simon WJ, Hall JJ (2006) Proteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics 6:845–864. doi:10.1002/pmic.200500196
Solomon A, Beer S, Waisel Y, Jones GP, Paleg LG (1994) Effects of NaCl on the carboxylating activity of Rubisco from Tamarix jordanis in the presence and absence of proline-related compatible solutes. Physiol Plant 90:198–204. doi:10.1034/J.1399-3054.1994.900128.X
Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803: the effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509:409–419. doi:10.1016/S0005-2736(00)00323-0
Takabe T, Rai V, Hibino T (2006) Metabolic engineering of glycinebetaine. In: Rai A, Takabe T (eds) Abiotic stress tolerance in plants: toward the improvement of global environment and food. Springer, Dordrecht, pp 137–151
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60. doi:10.1016/j.tplants.2010.10.001
Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochim Biophys Acta 1708:352–361. doi:10.1016/j.bbabio.2005.04.003
Takahashi S, Murata N (2006) Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757:198–205. doi:10.1016/j.bbabio.2006.02.002
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
Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255. doi:10.1093/pcp/pch028
Takahashi S, Bauwe H, Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144:487–494. doi:10.1104/pp. 107.097253
Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009a) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567. doi:10.1104/pp. 108.134122
Takahashi S, Whitney SM, Badger MR (2009b) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci U S A 106:3237–3242. doi:10.1073/pnas.0808363106
Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, Badger MR (2010) The solar action spectrum of photosystem II damage. Plant Physiol 153:988–993. doi:10.1104/pp. 110.155747
Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535. doi:10.1073/pnas.0402907101
Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917
Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376
Tyystjärvi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303. doi:10.1016/B978-0-12-405210-9.00007-2
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 U S A 93:2213–2218
Tyystjärvi E, Riikonen M, Arisi ACM, Kettunen R, Jouanin L, Foyer CH (1999) Photoinhibition of photosystem II in tobacco plants overexpressing glutathione reductase and poplars overexpressing superoxide dismutase. Physiol Plant 105:409–416. doi:10.1034/J.1399-3054.1999.150304.X
Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209–217. doi:10.1016/j.bbabio.2011.04.014
Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci U S A 89:1408–1412
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
Wada H, Gombos Z, Murata N (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc Natl Acad Sci U S A 91:4273–4277
Wang Y, Noguchi K, Ono N, Inoue S, Terashima I, Kinoshita T (2014) Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth. Proc Natl Acad Sci U S A 111:533–538. doi:10.1073/pnas.1305438111
Wei L, Guo J, Ouyang M, Sun X, Ma J, Chi W, Lu C, Zhang L (2010) LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J Biol Chem 285:21391–21398. doi:10.1074/jbc.M110.105064
Weis E (1981) Reversible heat inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151:33–39. doi:10.1007/Bf00384234
Weis E (1982) Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Plant Physiol 70:1530–1534. doi:10.1104/pp. 70.5.1530
Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc B 355:1517–1529
Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa T, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photo-oxidative stress. Plant J 32:915–925. doi:10.1046/j.1365-313X.2002.01476.x
Yamamoto Y, Inagaki N, Satoh K (2001) Overexpression and characterization of carboxy-terminal processing protease for precursor D1 protein: regulation of enzyme-substrate interaction by molecular environments. J Biol Chem 276:7518–7525. doi:10.1074/jbc.M008877200
Yang X, Liang Z, Lu C (2005) Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol 138:2299–2309. doi:10.1104/pp. 105.063164
Yang XH, Wen XG, Gong HM, Lu QT, Yang ZP, Tang YL, Liang Z, Lu CM (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733. doi:10.1007/S00425-006-0380-3
Zhang L, Aro EM (2002) Synthesis, membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II. FEBS Lett 512:13–18
Zheng CF, Jiang D, Liu FL, Dai TB, Jing Q, Cao WX (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582. doi:10.1016/j.plantsci.2009.01.015
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This work was supported, in part, by JSPS KAKENHI Grant Numbers 24570039 and 25119704 (to Y.N.).
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Nishiyama, Y., Murata, N. Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98, 8777–8796 (2014). https://doi.org/10.1007/s00253-014-6020-0
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DOI: https://doi.org/10.1007/s00253-014-6020-0