Skip to main content
SpringerLink
Log in

Heat stress: an overview of molecular responses in photosynthesis

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The primary targets of thermal damage in plants are the oxygen evolving complex along with the associated cofactors in photosystem II (PSII), carbon fixation by Rubisco and the ATP generating system. Recent investigations on the combined action of moderate light intensity and heat stress suggest that moderately high temperatures do not cause serious PSII damage but inhibit the repair of PSII. The latter largely involves de novo synthesis of proteins, particularly the D1 protein of the photosynthetic machinery that is damaged due to generation of reactive oxygen species (ROS), resulting in the reduction of carbon fixation and oxygen evolution, as well as disruption of the linear electron flow. The attack of ROS during moderate heat stress principally affects the repair system of PSII, but not directly the PSII reaction center (RC). Heat stress additionally induces cleavage and aggregation of RC proteins; the mechanisms of such processes are as yet unclear. On the other hand, membrane linked sensors seem to trigger the accumulation of compatible solutes like glycinebetaine in the neighborhood of PSII membranes. They also induce the expression of stress proteins that alleviate the ROS-mediated inhibition of repair of the stress damaged photosynthetic machinery and are required for the acclimation process. In this review we summarize the recent progress in the studies of molecular mechanisms involved during moderate heat stress on the photosynthetic machinery, especially in PSII.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ASP:

Ascorbate peroxidase

Chl:

Chlorophyll

GB:

Glycinebetaine

OEC:

Oxygen-evolving complex

PM:

Photosynthetic machinery

PSII:

Photosystem II

PSI:

Photosystem I

QTL:

Quantitative trait loci

RC:

Reaction center

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

    Article  PubMed  CAS  Google Scholar 

  • Al-Khatib K, Paulsen GM (1989) Enhancement of thermal injury to photosynthesis in wheat plants and thylakoids by high light intensity. Plant Physiol 90:1041–1048

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Feyziev YM, Ahmed A, Hayashi H, Aliev JA, Klimov VV et al (1996) Stabilization of oxygen evolution and primary electron transport reactions in photosystem II against heat stress with glycinebetaine and sucrose. J Photochem Photobiol 34:149–157. doi:10.1016/1011-1344(95)07276-4

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Yruela Y, Picorel R, Klimov VV (1997) Bicarbonate is an essential constituent of the water-oxidizing complex of photosystem II. Proc Natl Acad Sci USA 94:5050–5054. doi:10.1073/pnas.94.10.5050

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev Ja A, Klimov VV et al (2003) Glycine betaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49. doi:10.1078/0176-1617-00845

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Allen R (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054

    PubMed  CAS  Google Scholar 

  • Aminaka R, Taira Y, Kashino Y, Koike H, Satoh K (2006) Acclimation to the growth temperature and thermosensitivity of photosystem II in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol 47:1612–1621. doi:10.1093/pcp/pcl024

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi:10.1146/annurev.arplant.50.1.601

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Balint I, Bhattacharya J, Perelman A, Schatz D, Moskovitz Y, Keren N et al (2006) Inactivation of the extrinsic subunit of photosystem II, PsbU, in Synechococcus PCC 7942 results in elevated resistance to oxidative stress. FEBS Lett 580:2117–2122. doi:10.1016/j.febslet.2006.03.020

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Ford RC, Mitchell RAC, Millner PA (1984) Chloroplast thylakoid membrane fluidity and its sensitivity to temperature. Planta 161:375–380. doi:10.1007/BF00398729

    Article  CAS  Google Scholar 

  • Barua D, Downs CA, Hechthorn SA (2003) Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. Funct Plant Biol 30:1071–1079. doi:10.1071/FP03106

    Article  CAS  Google Scholar 

  • Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543. doi:10.1146/annurev.pp.31.060180.002423

    Article  Google Scholar 

  • Bondarava N, Beyer P, Krieger-Liszkay A (2005) Function of the 23 kDa extrinsic protein of photosystem II as a manganese binding protein and its role in photoactivation. Biochim Biophys Acta 1708:63–70. doi:10.1016/j.bbabio.2005.01.005

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448. doi:10.1126/science.218.4571.443

    Article  PubMed  Google Scholar 

  • Braun P, Greenberg BM, Scherz A (1990) D1–D2-cytochrome b559 complex from the aquatic plant Spirodela oligorchiza: correlation between complex integrity, spectroscopic properties, photochemical activity and pigment composition. Biochemistry 29:10376–10387. doi:10.1021/bi00497a012

    Article  PubMed  CAS  Google Scholar 

  • Bukhov NG, Carpentier R (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol Plant 110:279–285. doi:10.1034/j.1399-3054.2000.110219.x

    Article  CAS  Google Scholar 

  • Bukhov NG, Mohanty P (1999) Elevated temperature stress effects on photosystems: characterization and evaluation of the nature of heat induced impairments. In: Singhal GS, Renger G, Sopory SK, Irrgang K-D, Govingjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa Publishing House, New Delhi, pp 617–648

    Google Scholar 

  • Carpentier R (1999) Effect of high-temperature stress on the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker Inc, New York, pp 337–348

    Google Scholar 

  • Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L et al (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93:3870–3875. doi:10.1073/pnas.93.9.3870

    Article  PubMed  CAS  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaine and other compatible solutes. Curr Opin Plant Biol 5:250–257. doi:10.1016/S1369-5266(02)00255-8

    Article  PubMed  CAS  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97:13430–13435. doi:10.1073/pnas.230451497

    Article  PubMed  CAS  Google Scholar 

  • Dau H, Iuzzolino L, Dittmer J (2001) The tetramanganese complex of photosystem II during its redox cycle. X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503:24–39. doi:10.1016/S0005-2728(00)00230-9

    Article  PubMed  CAS  Google Scholar 

  • De Las Rivas J, Heredia P (1999) Structural predictions on the 33 kDa extrinsic protein associated with the oxygen evolving complex of photosynthetic organisms. Photosynth Res 61:11–21. doi:10.1023/A:1006265816104

    Article  Google Scholar 

  • Downs CA, Coleman JS, Heckathorn SA (1999) The chloroplast 22-kDa heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. J Plant Physiol 155:477–487

    CAS  Google Scholar 

  • El-Shitinawy F, Ebrahim MKH, Sewelam N, El-Shourbagy MN (2004) Activity of photosystem 2, lipid peroxidation, and the enzymatic antioxidant protective system in heat shocked barley seedlings. Photosynthetica 42:15–21. doi:10.1023/B:PHOT.0000040564.79874.42

    Article  Google Scholar 

  • 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 PS II 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

    Article  CAS  Google Scholar 

  • Enami I, Kamo M, Ohta H, Takahashi S, Miura T, Kusayanagi M, Tanabe S, Kamei A, Motoki A, Hirano M, Tomo T, Satoh K (1998) Intramolecular cross-linking of the extrinsic 33-kDa protein leads to loss of oxygen evolution but not its ability of binding to photosystem II and stabilization of the manganese cluster. J Biol Chem 273:4629–4634. doi:10.1074/jbc.273.8.4629

    Article  PubMed  CAS  Google Scholar 

  • Feller U, Crafts-Brandner SJ, Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-biphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116:539–546. doi:10.1104/pp.116.2.539

    Article  PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. doi:10.1126/science.1093087

    Article  PubMed  CAS  Google Scholar 

  • Gombos Z, Wada H, Murata N (1991) Direct evaluation of effects of fatty-acid unsaturation on the thermal properties of photosynthetic activities, as studied by mutation and transformation of Synechocystis PCC6803. Plant Cell Physiol 32:205–211

    CAS  Google Scholar 

  • Gombos Z, Wada H, Hideg E, Murata N (1994) The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiol 104:563–567

    PubMed  CAS  Google Scholar 

  • Gounaris K, Brain ARR, Quinn PJ, Williams WP (1983) Structural and functional changes associated with heat-induced phase separation of non-bilayer lipids in chloroplast thylakoid membranes. FEBS Lett 153:47–53. doi:10.1016/0014-5793(83)80117-3

    Article  CAS  Google Scholar 

  • Gounaris K, Brain ARR, Quinn PJ, Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766:198–208. doi:10.1016/0005-2728(84)90232-9

    Article  CAS  Google Scholar 

  • Hall AE (2001) Crop responses to environment. CRS Press LLC, Boca Raton, pp 324

  • Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467. doi:10.1111/j.1365-3040.1993.tb00893.x

    Article  Google Scholar 

  • Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333. doi:10.1007/BF00620047

    Article  CAS  Google Scholar 

  • Havaux M, Greppin H, Strasser RJ (1991) Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186:88–98. doi:10.1007/BF00201502

    Article  CAS  Google Scholar 

  • Heckathorn S, Downs SA, Sharkey TD, Soleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444. doi:10.1104/pp.116.1.439

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn SA, Ryan SL, Baylis JA, Wang D, Hamilton EW, Cundiff L et al (2002) In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct Plant Biol 29:933–944. doi:10.1071/PP01191

    Article  CAS  Google Scholar 

  • Hong SW, Vierling E (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27:25–35. doi:10.1046/j.1365-313x.2001.01066.x

    Article  PubMed  CAS  Google Scholar 

  • Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G et al (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a fluidity gene. Proc Natl Acad Sci USA 95:3513–3518. doi:10.1073/pnas.95.7.3513

    Article  PubMed  CAS  Google Scholar 

  • Inaba M, Grandall P (1988) Electrolyte leakage as an indicator of high-temperature injury to harvested mature green tomatoes. J Am Soc Hortic Sci 113:96–99

    Google Scholar 

  • Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H et al (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191–12198. doi:10.1074/jbc.M212204200

    Article  PubMed  CAS  Google Scholar 

  • Kalitulo LN, Pshybutko NL, Kabashnikova LF, Jahns P (2003) Photosynthetic apparatus and high temperature: role of light. Bulg J Plant Physiol 32:281–289

    Google Scholar 

  • Katoh S, San Pietro A (1967) Photooxidation and reduction of cytochrome-552 and NADP photoreduction by Euglena chloroplast. Arch Biochem Biophys 121:211–219. doi:10.1016/0003-9861(67)90026-4

    Article  PubMed  CAS  Google Scholar 

  • Kim K, Portis AR Jr (2004) Oxygen-dependent H2O2 production by rubisco. FEBS Lett 571:124–128. doi:10.1016/j.febslet.2004.06.064

    Article  PubMed  CAS  Google Scholar 

  • Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y, Hayashi H (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is also essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol 43:932–938. doi:10.1093/pcp/pcf110

    Article  PubMed  CAS  Google Scholar 

  • Klimov VV, Baranov SV, Allakhverdiev SI (1997) Bicarbonate protects the donor side of photosystem II against photoinhibition and thermoinactivation. FEBS Lett 418:243–246. doi:10.1016/S0014-5793(97)01392-6

    Article  PubMed  CAS  Google Scholar 

  • Komayama K, Khatoon M, Takenaka D, Horie J, Yamashita A, Yoshioka M et al (2007) Quality control photosystem II cleavage and aggregation of D1 protein in spinach thylakoids. Biochim Biophys Acta 1767:6830–6837

    Google Scholar 

  • Kreslavski VD, Khristin MS (2003) Aftereffect of heat shock on fluorescence induction and low-temperature fluorescence spectra of wheat leaves. Russ J Biophys 48:865–872

    Google Scholar 

  • Kreslavski VD, Balakhnina TI, Khristin MS, Bukhov NG (2001) Pretreatment of bean seedlings by choline compounds increases the resistance of photosynthetic apparatus to UV radiation and elevated temperatures. Photosynthetica 39:353–358. doi:10.1023/A:1015174108937

    Article  Google Scholar 

  • Kreslavski VD, Carpentier R, Klimov VV, Murata N, Allakhverdiev SI (2007) Molecular mechanisms of stress resistance of the photosynthetic apparatus. Membr Cell Biol 1:185–205

    Google Scholar 

  • Kreslavski V, Tatarinzev N, Shabnova N, Semenova G, Kosobrukhov A (2008) Characterization of the nature of photosynthetic recovery of wheat seedlings from short-time dark heat exposures and analysis of the mode of acclimation to different light intensities. J Plant Physiol. doi.org/10.1016/j.jplph.2007.12.011

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346. doi:10.1093/jxb/erh237

    Article  PubMed  CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695. doi:10.1104/pp.128.2.682

    Article  PubMed  CAS  Google Scholar 

  • Law R, 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 120:173–182. doi:10.1104/pp.120.1.173

    Article  PubMed  CAS  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157

    PubMed  CAS  Google Scholar 

  • Maestri E, Klueva N, Perrotta C, Gullil M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681. doi:10.1023/A:1014826730024

    Article  PubMed  CAS  Google Scholar 

  • Mamedov MD, Hayashi H, Murata N (1993) Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron transport and phosphorilation reactions in Synechocystis PCC 6803. Biochim Biophys Acta 1142:1–5. doi:10.1016/0005-2728(93)90077-S

    Article  CAS  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483. doi:10.1021/cr0204294

    Article  PubMed  CAS  Google Scholar 

  • Miyake C, Okamura M (2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant Cell Physiol 44:457–462. doi:10.1093/pcp/pcg053

    Article  PubMed  CAS  Google Scholar 

  • Mohanty P, Vani B, Prakash S (2002) Elevated temperature treatment induced alteration in thylakoid membrane organization and energy distribution between the two photosystems in Pisum sativum. Z Naturforsch 57:836–842

    CAS  Google Scholar 

  • Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperature during photoinhibition allows characterization of individual steps in photodamage and repair of photosystem II. Photosynth Res 94:217–234. doi:10.1007/s11120-007-9184-y

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879

    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. doi:10.1016/j.bbabio.2006.11.019

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838. doi:10.1105/tpc.105.031914

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301–308. doi:10.1104/pp.120.1.301

    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. doi:10.1093/emboj/20.20.5587

    Article  PubMed  CAS  Google Scholar 

  • 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

    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. doi:10.1016/j.bbabio.2006.05.013

    Article  PubMed  CAS  Google Scholar 

  • Nitta K, Suzuki N, Honma D, Kaneko Y, Nakamoto H (2005) Ultrastructural stability under high temperature or intensive light stress conferred by a small heat shock protein in cyanobacteria. FEBS Lett 579:1235–1242. doi:10.1016/j.febslet.2004.12.095

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pastenes C, Horton R (1996) Effect of high temperature on photosynthesis in beans. Plant Physiol 112:1245–1251

    PubMed  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks and pathways of cross-tolerance to stress. The central role of “redox” and abscisic-acid-mediated controls. Plant Physiol 129:460–468. doi:10.1104/pp.011021

    Article  PubMed  CAS  Google Scholar 

  • Pueyo JJ, Alfonso M, Andres C, Picorel R (2002) Increased tolerance to thermal inactivation of oxygen evolution in spinach photosystem II membranes by substitution of the extrinsic 33-kDa protein by its homologue from a thermophilic cyanobacterium. Biochim Biophys Acta 1554:22–35. doi:10.1016/S0005-2728(02)00207-4

    Article  Google Scholar 

  • Roose JL, Wegener KM, Pakrasi HB (2007) The extrinsic proteins of photosystem II. Photosynth Res 92:369–387. doi:10.1007/s11120-006-9117-1

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1046/j.0016-8025.2001.00790.x

    Article  PubMed  CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470. doi:10.1104/pp.103.038323

    Article  PubMed  CAS  Google Scholar 

  • Sato N, Sonoike K, Kawaguchi A, Tsuzuki M (1996) Contribution of lowered unsaturation levels of chloroplast lipids to high temperature tolerance of photosynthesis in Chlamydomonas reinhardtii. J Photochem Photobiol 36:333–337. doi:10.1016/S1011-1344(96)07389-7

    Article  CAS  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60. doi:10.1016/S0005-2728(96)00102-8

    Article  PubMed  Google Scholar 

  • Semenova GA (2004) Structural reorganization of thylakoid systems in response to heat treatment. Photosynthetica 42:521–527. doi:10.1007/S11099-005-0008-z

    Article  Google Scholar 

  • Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277. doi:10.1111/j.1365-3040.2005.01324.x

    Article  CAS  Google Scholar 

  • Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S et al (2008) The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal. EMBO J 27:782–791. doi:10.1038/emboj.2008.12

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. doi:10.1111/j.0031-9317.2005.00582.x

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Nishiyama Y, Murata N (2000) Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes. Plant Physiol 124:441–450. doi:10.1104/pp.124.1.441

    Article  PubMed  CAS  Google Scholar 

  • Török Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G et al (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103. doi:10.1073/pnas.051619498

    Article  PubMed  Google Scholar 

  • Vani B, Saradhi PP, Mohanty P (2001) Characterization of high temperature induced stress impairments in thylakoids of rice seedlings. Indian J Biochem Biophys 38:220–229

    PubMed  CAS  Google Scholar 

  • Vigh L, Maresca B, Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23:369–374. doi:10.1016/S0968-0004(98)01279-1

    Article  PubMed  CAS  Google Scholar 

  • Villarejo A, Shutova T, Moskvin O, Forssen M, Klimov VV, Samuelsson G (2002) A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution. EMBO J 21:1930–1938. doi:10.1093/emboj/21.8.1930

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 91:4273–4277. doi:10.1073/pnas.91.10.4273

    Article  PubMed  CAS  Google Scholar 

  • Wahid A, Shabbir A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Regul 46:133–141. doi:10.1007/s10725-005-8379-5

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223. doi:10.1016/j.envexpbot.2007.05.011

    Article  Google Scholar 

  • Weis E (1981) The temperature-sensitivity of dark inactivation and light activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett 129:197–200. doi:10.1016/0014-5793(81)80164-0

    Article  CAS  Google Scholar 

  • Yamada M, Hidaka T, Fukamachi H (1996) Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. Sci Hortic (Amsterdam) 67:39–48. doi:10.1016/S0304-4238(96)00931-4

    Article  CAS  Google Scholar 

  • Yamamoto H, Miyake C, Dietz K-J, Tomizawa K, Murata N, Yokota A (1999) Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 447:269–273. doi:10.1016/S0014-5793(99)00309-9

    Article  PubMed  CAS  Google Scholar 

  • Yamane Y, Shikanai T, Koike H, Satoh K (2000) Reduction of QA in the dark: another cause of fluorescence Fo increases by high temperatures in higher plants. Photosynth Res 63:23–34. doi:10.1023/A:1006350706802

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y et al (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

    Article  PubMed  CAS  Google Scholar 

  • Yordanov IS, Dilova R, Petkova T, Pangelova V, Goltsev V, Süss K-H (1986) Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem Photobiophys 12:147–155

    Google Scholar 

  • Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N et al (2006) Quality control of photosystem II. Cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J Biol Chem 281:21660–21669. doi:10.1074/jbc.M602896200

    Article  PubMed  CAS  Google Scholar 

  • Zharmukhamedov SK, Shirshikova GN, Maevskaya ZV, Antropova TM, Klimov VV (2007) Bicarbonate protects the water-oxidizing complex of photosystem II against thermoinactivation in intact Chlamydomonas reinhardtii cells. Russ J Plant Physiol 54:302–308. doi:10.1134/S1021443707030028

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported, in part, by grants from the Russian Foundation for Basic Research and from the Molecular and Cellular Biology Programs of the Russian Academy of Sciences. P.M. acknowledges the support of INSA, JNU, and DST/RAS (INT/ILTP/B-6.27). R.C. was supported by NSERC. The authors thank Dr. Anjana Jajoo for helpful discussion and reading the manuscript.

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, 142290, Russia

    Suleyman I. Allakhverdiev, Vladimir D. Kreslavski & Vyacheslav V. Klimov

  2. Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia

    Dmitry A. Los

  3. Groupe de Recherche en Biologie Végétale, Université du Québec à Trois-Rivières, C.P. 500, Quebec, Canada, G9A 5H7

    Robert Carpentier

  4. Regional Plant Resource Center, Nayapalli, Bhubaneswar, India

    Prasanna Mohanty

  5. Jawaharlal Nehru University, New Delhi, India

    Prasanna Mohanty

Authors
  1. Suleyman I. Allakhverdiev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladimir D. Kreslavski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vyacheslav V. Klimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dmitry A. Los
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert Carpentier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Prasanna Mohanty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suleyman I. Allakhverdiev.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Allakhverdiev, S.I., Kreslavski, V.D., Klimov, V.V. et al. Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98, 541–550 (2008). https://doi.org/10.1007/s11120-008-9331-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-008-9331-0

Keywords

Search

Navigation