Skip to main content
SpringerLink
Log in

Heat Stress: Susceptibility, Recovery and Regulation

  • Chapter
  • First Online:
Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 34))

Summary

The primary targets of thermal damage in plants are the oxygen-evolving complex and its associated cofactors in photosystem II (PS II), carbon fixation by Rubisco (Ribulose-1,5-bisphosphate carboxylase oxygenase) and the ATP generating system. The enzyme Rubisco activase is extremely sensitive to weak and moderate heat stress. Recent investigations on the combined action of moderate light intensity and heat stress suggest that moderately high temperatures do not cause serious PS II damage but inhibit the repair of PS II. 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 reduced rates of carbon fixation and oxygen evolution, as well as disruption of linear electron flow. The attack of ROS during moderate heat stress principally affects the repair system of PS II, but not directly the PS II reaction center. Heat stress additionally induces cleavage and aggregation of reaction center proteins and pigment-protein complexes, 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 PS II in thylakoid membranes. They also induce the expression of stress proteins that alleviate the ROS-mediated inhibition of stress damage repair of the photosynthetic machinery and are required for the acclimation process. In this chapter we summarize recent progress in the studies of molecular mechanisms involved during moderate heat stress on the photosynthetic machinery, especially in PS II and the CO2 assimilation system. We also examine joint effects of high temperature and other stress factors.

He is deceased. He lived from June 17, 1949 to February 8, 2011

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

APX –:

Ascorbate peroxidase;

Chl –:

Chlorophyll;

D1/D2/Cyt b 559 –:

Isolated Photosystem II complex retaining the D1 D2 and cytochrome b 559 proteins;

DF –:

Delayed fluorescence;

F –:

(chlorophyll) Fluorescence;

Fo – :

Basal (initial or minimal) (chlorophyll) fluorescence;

Fi –:

(chlorophyll) Fluorescence intensity at 30 ms;

Fv – :

Variable (chlorophyll) fluorescence;

Fm –:

Maximum (chlorophyll) fluorescence;

Fp –:

Maximum measured (chlorophyll) fluorescence intensity; Fp=Fm only when all PS II reaction centers are closed;

HSPs –:

Heat-shock proteins;

HSFs –:

Heat-shock (transcription) factors;

LHCII –:

Light-harvesting complex II;

OEC –:

Oxygen-evolving complex;

PS II –:

Photosystem II;

PS I –:

Photosystem I;

QTL –:

Quantitative trait loci;

ROS –:

Reactive oxygen species;

SOD –:

Superoxide dismutase

References

  • Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition: a historical perspective. Photosynth Res 76: 343–370

    Article  PubMed  CAS  Google Scholar 

  • Al-Khatib K and 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 and 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI and Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98: 529–539

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Klimov VV and Carpentier R (1994) Variable thermal emission and chlorophyll fluorescence in photosystem II particles. Proc Natl Acad Sci USA 91: 281–285

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Feyziev YM, Ahmed A, Hayashi H, Aliev JA, Klimov VV, Murata N and Carpentier R (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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Suzuki I, Tasaka Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I and Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol 125:1842–1853

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev Ja.A, Klimov VV, Murata N and Carpentier R (2003) Glycine betaine protects the D1/D2/Cytb 559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160: 41–49

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Mohanty P and Murata N (2004) 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

    Article  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I and Murata N (2005a) 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Tsvetkova N, Mohanty P, Szalontai B, Moon BY, Debreczeny M and Murata N (2005b) Irreversible photoinhibition of photosystem II is caused by exposure of Synechocystis cells to strong light for a prolonged period. Biochim Biophys Acta 1708: 342–351

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R and Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98: 541–550

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2004) Cytochrome b 6 f: structure for signalling and vectorial metabolism. Trends Plant Sci. 9: 130–137

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Alexciev K and Hakansson G (1995) Regulation of redox signalling. Curr Biol 5: 869–872

    Article  PubMed  CAS  Google Scholar 

  • Allen JF and Mullineaux CW (2004) Probing the mechanisms of state transitions in oxygenic photosynthesis by chlorophyll fluorescence spectroscopy: Kinetics and Imaging. In: Papageorgiou GC and Govindjee (eds) Chlorophyll a Fluroscence: a signature of Photosynthesis, Advances in Photosynthesis and Respiration, Vol 19, pp 447–461. Springer, Dodrecht

    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 and 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

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    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

    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

    Article  PubMed  CAS  Google Scholar 

  • Baker NR and Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55: 1607–1621

    Article  PubMed  CAS  Google Scholar 

  • Balint I, Bhattacharya J, Perelman A, Schatz D, Moskovitz Y, Keren N and Schwarz R (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

    Article  PubMed  CAS  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, et al. (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29: 471–487

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Barua D, Downs CA and 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

    Article  CAS  Google Scholar 

  • Berry JA and Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31: 491–543

    Article  Google Scholar 

  • Bonaventura C and Myers J (1969) Fluoresence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189: 366–383

    Article  PubMed  CAS  Google Scholar 

  • Bondarava N, Beyer P and 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

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218: 443–448

    Article  PubMed  CAS  Google Scholar 

  • Braun P, Greenberg BM and Scherz A (1990) D1-D2-Cytochrome b 559 complex from the aquatic plant Spirodela oligorchiza: Correlation between complex integrity, spectroscopic properties, photochemical activity and pigment composition. Biochemistry 29: 10376–10387

    Article  PubMed  CAS  Google Scholar 

  • Bukhov NG and 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 and Govindjee (eds) Concepts in Photobiology: Photosynthesis and Photomorphogenesis, pp 617–648. Narosa Publishing House, New Delhi

    Chapter  Google Scholar 

  • Bukhov NG and Carpentier R (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol Plant 110: 279–285

    Article  CAS  Google Scholar 

  • Bukhov NG, Boucher N and Carpentier R (1998) Loss of the precise control of photosynthesis and increased yield of nonradiative dissipation of excitation energy after mild heat treatment of barley leaves. Physiol Plant 104: 563–570

    Article  CAS  Google Scholar 

  • Cao J and Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive photosystem II in thylakoid membranes. Biochim Biophys Acta 1015: 180–189

    Article  PubMed  CAS  Google Scholar 

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

    Chapter  Google Scholar 

  • Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L and Maresca B (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

    Article  PubMed  CAS  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH and Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143: 251–262

    Article  PubMed  CAS  Google Scholar 

  • Chen THH and 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH and Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116: 1351–1357

    Article  PubMed  CAS  Google Scholar 

  • Dau H, Iuzzolino L and 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

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K and Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell, 17: 268–281

    Article  PubMed  CAS  Google Scholar 

  • De Las Rivas J and 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

    Article  CAS  Google Scholar 

  • Deshnium P, Los DA, Hayashi H, Mustardy L and Murata N (1995) Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol : 897–907

    Article  PubMed  CAS  Google Scholar 

  • Dietzel L, Bräutigam K and Pfannschmidt T (2008) Photosynthetic acclimation: state transition adjustment of photosystem stoichiometry – functional relationship between short-term and long-term acclimation. FEBS J 275: 1080—1088

    Article  PubMed  CAS  Google Scholar 

  • Downs CA, Coleman JS and 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

    Article  CAS  Google Scholar 

  • El-Shitinawy F, Ebrahim MKH, Sewelam N and 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

    Article  Google Scholar 

  • Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H and 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

    Article  CAS  Google Scholar 

  • Enami I, Kamo M, Ohta H, Takahashi S, Miura Taro, Kusayanagi M, Tanabe S, Kamei A, Motoki A, Hirano M, Tomo T and 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF and Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100: 241–254

    Article  CAS  Google Scholar 

  • Goltsev V, Zaharieva I, Chernov P and Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101: 217–232

    Article  PubMed  CAS  Google Scholar 

  • Gombos Z, Wada H and 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 and 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 and 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

    Article  CAS  Google Scholar 

  • Gounaris K, Brain ARR, Quinn PJ and Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766: 198–208

    Article  CAS  Google Scholar 

  • Govindachary S, Bigras C, Harnois J, Joly D and Carpentier R (2007) Changes in the mode of electron flow to photosystem I following chilling-induced photoinhibition in a C3 plant, Cucumus sativus L. Photosynth Res 94: 333–345

    Article  PubMed  CAS  Google Scholar 

  • Govindjee (2004) Chlorophyll a fluorescence: a bit of basics and history. In Papageorgiou GC and Govindjee (eds) Chlorophyll a Fluorescence: A Signature of Photo­synthesis, Advances in Photosynthesis and Respiration, Vol 19, pp 1–42. Springer, Dordrecht

    Chapter  Google Scholar 

  • Guisse B, Srivastava A and Strasser RJ (1995) The polyphasic rise of chlorophyll a fluorescence (OKIJP) in heat stressed leaves. Arch Sci Geneve 48: 147–160

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hall AE (2001) Crop Responses to Environment. CRS press LLC, Boca Raton

    Google Scholar 

  • Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16: 461–467

    Article  Google Scholar 

  • Havaux M and 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

    Article  CAS  Google Scholar 

  • Havaux M, Greppin H and 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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn SA, Ryan SL, Baylis JA, Wang D, Hamilton EW, Cundiff L and Luthe DS (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

    Article  CAS  Google Scholar 

  • Hecker M, Schumann W and Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19: 417–428

    Article  PubMed  CAS  Google Scholar 

  • Hong SW and 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

    Article  PubMed  CAS  Google Scholar 

  • Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F and Vigh L (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

    Article  PubMed  CAS  Google Scholar 

  • Joshi MK, Deasai TS and Mohanty P (1995) Temperature dependent alterations in the pattern of photochemical and nonphotochemical quenching and associated changes in the photosystem II conditions of the leaves. Plant Cell Physiol 36: 1221–1227

    CAS  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Joliot P and Joliot A (1980) Dependence of delayed luminescence upon adenosine triphosphatase activity in Chlorella. Plant Physiol 65: 691–696

    Article  PubMed  CAS  Google Scholar 

  • Jones PD, New M, Parker DE, Mortin S and Rigor IG (1999) Surface area temperature and its change over the past 150 years. Rev Geophys 37: 173–199

    Article  Google Scholar 

  • Jursinic P (1986) Delayed fluorescence: Current concepts and status. In: Govindjee, Amesz J, Fork DJ (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 291–328

    Google Scholar 

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

    Google Scholar 

  • Katoh S and San Pietro A (1967) Photooxidation and reduction of cytochrome-552 and NADP photoreduction by Euglena chloroplast. Arch Biochem Biophys 121: 211–219

    Article  PubMed  CAS  Google Scholar 

  • Kim K and Portis AR (Jr) (2004) Oxygen-dependent H2O2 production by rubisco. FEBS Lett 571: 124–128

    Article  PubMed  CAS  Google Scholar 

  • Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Klimov VV, Baranov SV and Allakhverdiev SI (1997) Bicarbonate protects the donor side of photosystem II against photoinhibition and thermoinactivation. FEBS Lett 418: 243–246

    Article  PubMed  CAS  Google Scholar 

  • Klimov VV, Allakhverdiev SI, Nishiyama Y, Khorobrykh AA and Murata N (2003) Stabilization of the oxygen-evolving complex of photosystem II by bicarbonate and glycinbetaine in thylakoid and subthylakoid preparations. Fun Plant Biol 30: 797–803

    Article  CAS  Google Scholar 

  • Kojima K and 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 

  • Komayama K, Khatoon M, Takenaka D, Horie J, Yamashita A, Yoshioka M, Nakayama Y, Yoshida M, Ohira S, Morita N, Velitchkova M, Enami I and Yamamoto Y (2007) Quality control of Photosystem II: cleavage and aggregation of heat-damaged D1 protein in spinach thylakoids. Biochim Biophys Acta 1767: 838–846

    Article  PubMed  CAS  Google Scholar 

  • Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V and Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination J Biol Chem 283: 34197–34203

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Kreslavski VD, Balakhnina TI, Khristin MS and 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

    Article  Google Scholar 

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

    Google Scholar 

  • Kreslavski V, Tatarinzev N, Shabnova N, Semenova G and 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 165: 1592–1600

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Larkindale J and 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

    Article  PubMed  CAS  Google Scholar 

  • Lavergne J and Leci E (1993) Properties of inactive photosystem II centers. Photosynth Res 35: 323–343

    Article  CAS  Google Scholar 

  • Lavorel J (1975) Luminescence. In: Govindjee (ed) Bioenergetics of Photosynthesis. Academic Press, New York, pp 223–317

    Google Scholar 

  • Law R and 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

    Article  PubMed  CAS  Google Scholar 

  • Lazar D (1999) Chorophyll a fluorescence induction. Biochim Biophys Acta 1412: 1–26

    Article  PubMed  CAS  Google Scholar 

  • Lazar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Functional Plant Biol 33: 9–30

    Article  CAS  Google Scholar 

  • Li H, Yang S, Xie J and Zhau J (2007) Probing the connection of PBSs to photosystems in Spirulina platensis by artificially induced fluorescence fluctuations. J Lumin 122/123: 294–296

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Los DA, Suzuki I, Zinchenko VV and Murata N (2008) Stress responses in Synechocystis: regulated genes and regulatory systems. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp 117–157. Caister Academic Press, London

    Google Scholar 

  • Lu C, Qiu N, Wang B and Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54: 851–860

    Article  PubMed  CAS  Google Scholar 

  • Lubben TH and Keegstra K (1986) Efficient in vitro import of a cytosolic heat shock protein into pea chloroplasts. Proc Natl Acad Sci USA 83: 5502–5506

    Article  PubMed  CAS  Google Scholar 

  • Maestri E, Klueva N, Perrotta C, Gulli1 M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48: 667–681

    Article  PubMed  CAS  Google Scholar 

  • Mamedov MD, Hayashi H and 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

    Article  CAS  Google Scholar 

  • McEvoy JP and Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106: 4455–4483

    Article  PubMed  CAS  Google Scholar 

  • Miller G and Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98: 279–288

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitsky S and Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144: 1777–1785

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci.7: 405–410

    Article  PubMed  CAS  Google Scholar 

  • Miyake C and 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

    Article  PubMed  CAS  Google Scholar 

  • Mohanty N, Murthy SD and Mohanty P (1987) Riversal of heat induced alteration in photochemical activities in wheat primary leaves. Photosyn Res 14: 259–267

    Article  CAS  Google Scholar 

  • Mohanty P (2008) Perspective of membrane perception of temperature. Physiol Mol Biol Plants 14: 273–275

    Article  CAS  Google Scholar 

  • Mohanty P, Munday JC and Govindjee (1970) Time dependent quenching of chlorophyll a fluorescence from (pigment) system II by (pigment) system I of photosynthesis in Chlorella. Biochim Biophys Acta 223: 198–200

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mohanty P, Allakhverdiev SI and 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

    Article  PubMed  CAS  Google Scholar 

  • Mubarakshina M, Khorobrykh S and Ivanov B (2006) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane. Biochim Biophys Acta 1757: 1496–1503

    Article  PubMed  CAS  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis: Light induced chlorophyll a fluorescence in Prophyridium cruentum. Biochim.Biophys Acta 172: 242–251

    Article  PubMed  CAS  Google Scholar 

  • Murata N (2009) The discovery of state transitions in photosynthesis 40 years ago. Photosynth Res. 99: 155–160

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai TL, Rutherford AW, Sugiura M, Boussac A and Barber J (2008) X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of photosystem II. Energy Environ Sci 1: 161–166

    Article  CAS  Google Scholar 

  • Nakamoto H, Suzuki M and Kojima K (2003) Targeted inactivation of the hrcA repressor gene in cyanobacteria. FEBS Lett 549: 57–62

    Article  PubMed  CAS  Google Scholar 

  • Nash D, Miyao M and 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

    Article  CAS  Google Scholar 

  • Neta-Sharir I, Isaacson T, Lurie S and 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

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Los DA and 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

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A and 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, Yamamoto H, Hayashi H and 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

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI and Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84: 1–7

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI and 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 

  • Nitta K, Suzuki N, Honma D, Kaneko Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Oh JI and Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbial 39: 1116–1123

    Article  CAS  Google Scholar 

  • Ohnishi N and 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

    Article  PubMed  CAS  Google Scholar 

  • Papageorgiou GC and Govindjee (1967) Changes in intensity and spectral distribution of fluorescence effect of light treatment on normal and DCMU poisoned Anasystis nidulans. Boophysical J 7: 375–389

    Article  CAS  Google Scholar 

  • Papageorgiou GC and Govindjee (eds) (2004) Chlorophyll a Fluorescence: A Signature of Photosynthesis, Advances in Photosynthesis and Respiration Series, Vol 19, Springer, Dordrecht

    Google Scholar 

  • Papageorgiou GC and Govindjee (2011) Photosystem II fluorescence: Slow changes -Scaling from the past. J Photochem Photobiol B:Biol104: 258–270

    Google Scholar 

  • Papageorgiou GC and 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

    Article  CAS  Google Scholar 

  • Papageorgiou GC, Tsimilli-Michael M and Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint Photosynth Res 94: 275–290

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pastori GM and 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

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8: 33–41

    Article  PubMed  CAS  Google Scholar 

  • Pshybytko NL, Jerzy Kruk J, Kabashnikova LF and Strzalka K (2008) Function of plastoquinone in heat stress reactions of plants. Biochim Biophys Acta. 1777: 1393–1470

    Article  PubMed  CAS  Google Scholar 

  • Pueyo JJ, Alfonso M, Andres C and 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

    Article  Google Scholar 

  • Roose JL, Wegener KM and Pakrasi HB (2007) The extrinsic proteins of Photosystem II. Photosynth Res 92: 369–387

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto A and 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

    Article  PubMed  CAS  Google Scholar 

  • Salvucci ME and 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

    Article  PubMed  CAS  Google Scholar 

  • Sane PV, Desai TS, Tatake VG and Govindjee (1984) Heat-induced reversible increase in photosystem I emission in algae, leaves and chloroplasts: spectra, activities, and relation to state changes. Photosynthetica 18: 439–444

    Google Scholar 

  • Sato N, Sonoike K, Kawaguchi A and 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

    Article  CAS  Google Scholar 

  • Sazanov LA, Borrows PA and Nixon PJ (1998) The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett 429: 115–118

    Article  PubMed  CAS  Google Scholar 

  • Schär C, Vidale PL, Lüthi D, Frei C, Häberli C and Liniger MA (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427: 332–336

    Article  PubMed  CAS  Google Scholar 

  • Schroda M, Vallon O, Wollman F-A and 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: 1165–178

    PubMed  CAS  Google Scholar 

  • Seidler A (1996) The extrinsic polypeptides of Photosystem II. Biochim Biophys Acta 1277: 35–60

    Article  PubMed  Google Scholar 

  • Semenova GA (2004) Structural reorganization of thylakoid systems in response to heat treatment. Photosynthetica 42: 521–527

    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 Env 28: 269–277

    Article  CAS  Google Scholar 

  • Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S, Andersson B, Allakhverdiev SI, Klimov VV, Dau H, Junge W and Samuelsson G (2008) The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal. EMBO J 27: 782–791

    Article  PubMed  CAS  Google Scholar 

  • Singh A and Grover A (2008) Genetic engineering for heat tolerance in plants. Physiol Mol Biol Plant 14: 155–166

    Article  CAS  Google Scholar 

  • Singh AK, Summerfield TC, Li H and Sherman LA (2006) The heat shock response in the cyanobacterium Synechocystis sp. strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol 186: 273–286

    Article  PubMed  CAS  Google Scholar 

  • Slabas AR, Suzuki I, Murata N, Simon WJ and Hall JJ (2006) Proteomic analysis of the heat shock response in Synechocystis PCC 6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene. Proteomics 6: 845–864

    Article  PubMed  CAS  Google Scholar 

  • Srivastava A, Guisse B, Greppin H and Strasser RJ (1997) Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature as probed bythe fast polyphasic chlorophyll a fluorescence transient OKJIP. Biochim Biophys Acta 1320: 95–106

    Article  CAS  Google Scholar 

  • Srivastava A, Strasser RJ and Govindjee (1995) Differential effects of dimethylquinone and dichlorobenzoquinone on chlorophyll fluorescence transient in spinach thylakoids. J Photochem Photobiol 31: 163–169

    Article  CAS  Google Scholar 

  • Stirbet A and Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B:Biol 104: 236–257

    Google Scholar 

  • Strasser BJ (1997) Donor side capacity of PSII probed by chlorophyll a fluorescence transients. Photosynth Res 52: 147–155

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli–Michael M and Srivastava A (2004) Analysis of chlorophyll a fluorescence transient In: Papageorgiou GG and Govindjee (eds) Chlrophyll a Fluroscence: A Signature of Photosynthesis, Advances in Photosynthesis and Respiration, Vol 19, pp 322–358. Springer, Dodrecht

    Google Scholar 

  • Strehler BL and Arnold W (1951) Light production by green plants. J Gen Physiol 34: 809–820

    Article  PubMed  CAS  Google Scholar 

  • Sung DY, Kaplan F, Lee KJ and Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8: 179–187

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR and 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 

  • Suzuki N and Mittler R (2006) Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol Plant 126: 45–51

    Article  CAS  Google Scholar 

  • Takahashi S and Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13: 178–182

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Nishiyama Y and 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

    Article  PubMed  CAS  Google Scholar 

  • Tang Y, Wen X, Lu O, Yang Z, Cheng Z and Lu C (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant Physiol 143: 629–638

    Article  PubMed  CAS  Google Scholar 

  • Tsimilli-Michael M, Stamatakis K and Papageorgiou GC (2009) Dark to light transition in Synechoccus sp. PCC 7942 cells studied by fluorescence kinetics asseses plastoquinone redox poise and photosytem II coimponents and dynamics during state 2 to state 1 transition. Photosynth Res 90: 243–255

    Article  CAS  Google Scholar 

  • Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K and Murata N (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

    PubMed  CAS  Google Scholar 

  • Török Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH and Vigh L (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

    Article  PubMed  Google Scholar 

  • Toth SZ, Schsanker G, Kissiam J, Garab G and Strasser RJ (2005) Biophysical studies of photosystem II related recovery processes after a heat pulse. J Pant Physiol 162: 181–194

    Article  CAS  Google Scholar 

  • Vani B, Mohanty P, Eggenberg P, Strasser B and Strasser RJ (1999) Heat stress on rice leaves probed by chlorophyll a fluorescence transient OKJIP. In: Garab G (ed) Photosynthesis: Effects and Mechanisms, pp 3837–3840. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Vani B, Saradhi PP and 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 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579–620

    Article  CAS  Google Scholar 

  • Vierling E, Mishkind ML, Schmidt GW and Key JL (1986) Specific heat shock proteins are transported into chloroplasts. Proc Natl Acad Sci USA 83: 361–365

    Article  PubMed  CAS  Google Scholar 

  • Vigh L, Maresca B and Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23: 369–374

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Volkov R, Panchuk I, Mullineaux P and Schoffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61: 733–746

    Article  PubMed  CAS  Google Scholar 

  • Wada H, Gombos Z and 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

    Article  PubMed  CAS  Google Scholar 

  • Wahid A and Shabbir A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine. Plant Growth Reg 46: 133–141

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Wang J, Xing D, Zhang L and Jia L (2007) A new principle photosynthesis capacity biosensor based on quantitative measurement of fluorescence in vivo. Biosen Bioelect 22: 2861–2868

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Wen X, Qiu N, Lu Q and Lu C (2005) Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. Plants 220: 486–497

    Article  CAS  Google Scholar 

  • Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F and Huner NPA (2006) Energy balance, organellar redox status, and acclimation to environmental stress. Can J Bot 84: 1355–1370

    Article  CAS  Google Scholar 

  • Yamada M, Hidaka T and Fukamachi H (1996) Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. Scientia Hortic 67: 39–48

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yamane Y, Shikanai T, Koike H and 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

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Liang Z and 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

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z and Lu C (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225: 719–733

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Yordanov I, Goltsev V, Stoyanova T and Venediktov P (1987) High-temperature damage and acclimation of the photosynthetic apparatus. I. Temperature sensitivity of some photosynthetic parameters of chloroplasts isolated from acclimated and non-acclimated bean leaves. Planta 170: 471–477

    Article  Google Scholar 

  • Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, Morita N, Nakanishi T and Yamamoto Y (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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We warmly thank Prof. V.V. Zinchenko for information on transcription factors in Synechocystis sp. PCC 6803, and Professors Govindjee and J. Eaton-Rye for many useful discussions. 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 to DAL, VVK and SIA, by a Grant-in-Aid for Creative Scientific Research (No. 17GS0314) from the Japanes Society for the Promotion of Science (JSPS) and by Scientific Research on Priority Areas “Comparative Genomics” (Nos: 17018022 and 18017016) from the Ministry of Education, Sports, Culture, Science, and Technology, Japan, to MM. PM acknowledges the support of Indian National Science Academy, Jawaharlal Nehru University and Department of Science and Technology of India and Russian Academy of Sciences (INT/ILTP/B-6.1 and 6.27). RC was supported by NSERC.

Author information

Authors and Affiliations

  1. Regional Plant Resource Center, Nayapalli, Bhubaneswar, 751015, India

    Prasanna Mohanty

  2. Jawaharlal Nehru University, New Delhi, 11006, India

    Prasanna Mohanty

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

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

  4. Institute of Plant Physiology, Russian Academy of Sciences, Moscow, 127276, Russia

    Dmitry A. Los & Suleyman I. Allakhverdiev

  5. Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, 606-8501, Japan

    Mamoru Mimuro

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

    Robert Carpentier

Authors
  1. Prasanna Mohanty
    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. Mamoru Mimuro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Carpentier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Suleyman I. Allakhverdiev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suleyman I. Allakhverdiev .

Editor information

Editors and Affiliations

  1. Dept. Biochemistry, University of Otago, Dunedin, New Zealand

    Julian J. Eaton-Rye

  2. School of Life Sciences, University of New Delhi, New Delhi, 110067, India

    Baishnab C. Tripathy

  3. Biochemistry Building 410, East Lansing, 48824, Michigan, USA

    Thomas D. Sharkey

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Mohanty, P. et al. (2012). Heat Stress: Susceptibility, Recovery and Regulation. In: Eaton-Rye, J., Tripathy, B., Sharkey, T. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 34. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1579-0_12

Download citation

Publish with us

Policies and ethics

Search

Navigation