Skip to main content
Log in

Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Under a moderately heat-stressed condition, the photosystems of higher plants are damaged in the dark more easily than they are in the presence of light. To obtain a better understanding of this heat-derived damage mechanism that occurs in the dark, we focused on the involvement of the light-independent electron flow that occurs at 40 °C during the damage. In various plant species, the maximal photochemical quantum yield of photosystem (PS) II (F v/F m) decreased as a result of heat treatment in the dark. In the case of wheat, the most sensitive plant species tested, both F v/F m and oxygen evolution rapidly decreased by heat treatment at 40 °C for 30 min in the dark. In the damage, specific degradation of D1 protein was involved, as shown by immunochemical analysis of major proteins in the photosystem. Because light canceled the damage to PSII, the light-driven electron flow may play a protective role against PSII damage without light. Light-independent incorporation of reducing power from stroma was enhanced at 40 °C but not below 35 °C. Arabidopsis mutants that have a deficit of enzymes which mediate the incorporation of stromal reducing power into thylakoid membranes were tolerant against heat treatment at 40 °C in the dark, suggesting that the reduction of the plastoquinone pool may be involved in the damage. In conclusion, the enhanced introduction of reducing power from stroma into thylakoid membranes that occurs around 40 °C causes over-reduction of plastoquinone, resulting in the damage to D1 protein under heat stress without linear electron flow.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

CBB:

Coomassie Brilliant Blue

CEF:

Cyclic electron flow

Fd:

Ferredoxin

FNR:

Fd-NADPH reductase

F v/F m :

Maximal photochemical quantum yield of photosystem II

NDH:

NAD(P)H dehydrogenase

NPQ:

Non-photochemical quenching

OEC:

Oxygen-evolution complex

OEC33:

OEC 33 kDa protein

PQ:

Plastoquinone

PS:

Photosystem

ROS:

Reactive oxygen species

References

  • Adir N, Shochat S, Ohad I (1990) Light-dependent D1 protein-synthesis and translocation is regulated by reaction center II: reaction center II serves as an acceptor for the D1 precursor. J Biol Chem 265:12563–12568

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Barber J, Kühlbrandt V (1999) Photosystem II. Curr Opin Struc Biol 9:469–475

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93

    Article  CAS  Google Scholar 

  • De Las Rivas J, Andersson B, Barber J (1992) Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in photosystem II core complexes. FEBS Lett 301:246–252

    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

    Article  CAS  Google Scholar 

  • Haldrup A, Lunde C, Scheller HV (2003) Arabidopsis thaliana plants lacking the PSI-D subunit of photosystem I suffer severe photoinhibition, have unstable photosystem I complexes, and altered redox homeostasis in the chloroplast stroma. J Biol Chem 278:33276–33283

    Article  PubMed  CAS  Google Scholar 

  • Havaux M (1996) Short-term responses of photosystem I to heat stress: Induction of a PS II-independent electron transport through PS I fed by stromal components. Photosynth Res 47:85–97

    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: analysis using in vivo fluorescence, absorbency, oxygen and photoacoustic measurements. Planta 186:88–98

    Article  CAS  Google Scholar 

  • Johnson GN, Boussac A, Rutherford W (1994) The origin of 40–50 °C thermoluminescence bands in photosystem II. Biochim Biophys Acta 1184:85–92

    Article  CAS  Google Scholar 

  • June T, Evans JR, Farquhar GD (2004) A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. Funct Plant Biol 31:275–283

    Article  CAS  Google Scholar 

  • Keren N, Berg A, van Kan PJM, 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 USA 94:1579–1584

    Article  PubMed  CAS  Google Scholar 

  • Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A (2004) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lintala M, Allahverdiyeva Y, Kangasjaärvi S, Lehtimäki N, Keränen M, Rintamäki E, Aro EM, Mulo P (2009) Comparative analysis of leaf-type ferredoxin-NADP+ oxidoreductase isoforms in Arabidopsis thaliana. Plant J 57:1103–1115

    Article  PubMed  CAS  Google Scholar 

  • Miranda T, Ducruet JM (1995) Characterization of the chlorophyll thermoluminescence afterglow in dark-adapted or far-red-illuminated plant-leaves. Plant Physiol Biochem 33:689–699

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Oelmüller R, Herrmann RG, Pakrasi HB (1996) Molecular studies of CtpA, the carboxyl-terminal processing protease for the D1 protein of the photosystem II reaction center in higher plants. J Biol Chem 271:21848–21852

    Article  PubMed  Google Scholar 

  • Ohira S, Morita N, Suh HJ, Jung J, Yamamoto Y (2005) Quality control of photosystem II under light stress: turnover of aggregates of the D1 protein in vivo. Photosynth Res 84:29–33

    Article  PubMed  CAS  Google Scholar 

  • Pospíšil P, Šnyrychová I, Nauš J (2007) Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature: EPR spin-trapping study. Biochim Biophys Acta 1767:854–859

    Article  PubMed  Google Scholar 

  • Rumeau D, Bécuwe-Linka N, Beyly A, Louwagie M, Garin J, Peltier G (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17:219–232

    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

    Article  PubMed  CAS  Google Scholar 

  • Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant, Cell Environ 27:725–735

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    Article  PubMed  CAS  Google Scholar 

  • Sundby C, Andersson B (1985) Temperature-induced reversible migration along the thylakoid membrane of photosystem II regulates its association with LHC-II. FEBS Lett 191:24–28

    Article  CAS  Google Scholar 

  • Vass I, Styring S, Hundall T, Koivuniemi A, Aro E-M, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89:1408–1412

    Article  PubMed  CAS  Google Scholar 

  • Weis E (1981) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151:33–39

    Article  CAS  Google Scholar 

  • Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K, Takenaka D, Yamashita A, Nijo N, Inagawa K, Morita N, Sasaki T (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth Res 98:589–608

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Peng L, Fukao Y, Shikanai T (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23:1480–1493

    Article  PubMed  CAS  Google Scholar 

  • Yamane Y, Kashino Y, Koike H, Satoh K (1998) Effects of high temperatures on the photosynthetic systems in spinach: oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynth Res 57:51–59

    Article  CAS  Google Scholar 

  • Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S (2002) Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiol 128:1087–1097

    Article  PubMed  CAS  Google Scholar 

  • Yamashita A, Nijo N, Pospíšil P, Morita N, Takenaka D, Aminaka R, Yamamoto Y (2008) Quality control of photosystem II: reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress. J Biol Chem 283:28380–28391

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Sugimoto Y (2010) Effect of protein modification by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins. Planta 231:1077–1088

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a Grant-in-Aid for Exploratory Research (Y.Y., 21658112) and Grant-in-Aid for Scientific Research (Y.Y., 23580456) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasuo Yamauchi.

Additional information

The authors Y. Marutani and Y. Yamauchi contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 525 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marutani, Y., Yamauchi, Y., Kimura, Y. et al. Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta 236, 753–761 (2012). https://doi.org/10.1007/s00425-012-1647-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1647-5

Keywords

Navigation