Skip to main content
SpringerLink
Log in

Responses of photosystem II photochemistry and the alternative oxidase pathway to heat stress in grape leaves

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

To study the photochemical responses of photosystem II (PSII) and mitochondrial alternative oxidase (AOX) to heat stress in grapevine (Vitis vinifera L. cv. ‘Cabernet Sauvignon’), we exposed grape leaves to a range of temperatures (25, 30, 35, 40, and 42.5 °C) in the light (600 µmol m−2 s−1). At temperatures >35 °C, the rate of photosynthetic O2 evolution and the maximal photochemistry efficiency of PSII (Fv/Fm) decreased significantly. We observed that the relative variable fluorescence increased at the J step, and there was also an accumulation of H2O2. In addition, there was an increase in both the non-photochemical quenching (NPQ) and the capacity of the alternative oxidase pathway (AOX) at higher temperatures. When the leaves were treated with the AOX inhibitor salicylhydroxamic acid, a significant decrease in the PSII electron transport rate and NPQ and an increase in H2O2 content occurred. Our results suggest that high temperature limits electron transport beyond Q −A , resulting in a strong accumulation of H2O2 in grape leaves. Inhibition of the AOX pathway increases the formation and accumulation of H2O2 in grape leaves, and may thereby increase photoinhibition in leaves experiencing heat stress.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

AOX:

Alternative oxidase

PSII:

Photosystem II

ROS:

Reactive oxygen species

SHAM:

Salicylhydroxamic acid

References

  • Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bartoli CG, Gomez F, Gergoff G, Guiamét JJ, Puntarulo S (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J Exp Bot 56:1269–1276

    Article  CAS  PubMed  Google Scholar 

  • Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol. 59: 411–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukhov NG, Samson G, Carpentier R (2000) Nonphotosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress. Steady-state rate. Photochem Photobiol 72:351–357

    Article  CAS  PubMed  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 97:13430–13435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99:197–209

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    Article  CAS  PubMed  Google Scholar 

  • Jiang CD, Gao HY, Zou Q (2001) Enhanced thermal energy dissipation depending on xanthophyll cycle and D1 protein turnover in iron-deficient maize leaves under high irradiance. Photosynthetica 39:269–274

    Article  CAS  Google Scholar 

  • Jiang CD, Jiang GM, Wang X, Li LH, Biswas DK, Li YG (2006) Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP. Environ Exp Bot 58:261–268

    Article  CAS  Google Scholar 

  • Ledford HK, Niyogi KK (2005) Singlet oxygen and photo-oxidative stress management in plants and algae. Plant Cell Environ 28:1037–1045

    Article  CAS  Google Scholar 

  • Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biol 13:1–6

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol 50:333–359

    Article  CAS  Google Scholar 

  • Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8:87–99

    Article  CAS  PubMed  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic Publishers, Dordrecht, pp 977–980

    Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Tóth SZ, Schansker G, Garab G, Strasser RJ (2007) Photosynthetic electron transport activity in heat-treated barley leaves: the role of internal alternative electron donors to photosystem II. Biochim Biophys Acta 1767:295–305

    Article  PubMed  Google Scholar 

  • Xu CC, Li L, Kuang T (2000) The inhibited xanthophyll cycle is responsible for the increase in sensitivity to low temperature photoinhibition in rice leaves fed with glutathione. Photosynth Res 65:107–114

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. J Plant Physiol 167:959–966

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Environ 48(4):606–614

    Article  CAS  Google Scholar 

  • Zhang L, Liu J (2015) Effects of heat stress on photosynthetic electron transport in a marine cyanobacterium Arthrospira sp. J Appl Phycol 28:1–7

    Google Scholar 

  • Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407

    Article  CAS  PubMed  Google Scholar 

  • Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng QW (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Wang X, Wang X, Wu K, Li P, Chang N, Wang J, Wang F, Li J, Bi Y (2015) Glucose-6-phosphate dehydrogenase and alternative oxidase are involved in the cross tolerance of highland barley to salt stress and UV-B radiation. J Plant Physiol 181:83–95

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the China Agriculture Research System (CARS-30) and the Program for Yangtze River Scholars and Innovative Research Team in University (PCSIRT1155).

Author information

Authors and Affiliations

  1. College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, Shandong, 271018, China

    Yongjiang Sun, Xiaohong Liu, Heng Zhai, Yuxin Yao & Yuanpeng Du

  2. State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an, Shandong, 271018, China

    Huiyuan Gao

Authors
  1. Yongjiang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaohong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heng Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huiyuan Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuxin Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuanpeng Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heng Zhai.

Additional information

Communicated by U. Feller.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, Y., Liu, X., Zhai, H. et al. Responses of photosystem II photochemistry and the alternative oxidase pathway to heat stress in grape leaves. Acta Physiol Plant 38, 232 (2016). https://doi.org/10.1007/s11738-016-2235-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2235-2

Keywords

Search

Navigation