Photosynthetica, 2018 (vol. 56), issue 4

Photosynthetica 2018, 56(4):1297-1303 | DOI: 10.1007/s11099-018-0837-1

Role of alternative oxidase pathway in protection against drought-induced photoinhibition in pepper leaves

W. H. Hu1,*, X. H. Yan1, Y. He2, X. L. Ye1
1 School of Life Sciences, Jinggangshan University, Ji'an, China
2 Jiujiang Agricultural Bureau, Jiujiang, China

The aim of this study was to assess the impact of the mitochondrial alternative oxidase (AOX) pathway on energy metabolism in chloroplasts, and evaluate the importance of the AOX in alleviating drought-induced photoinhibition in pepper (Capsicum annuum L.). Inhibition of AOX pathway decreased photosynthesis and increased thermal energy dissipation in plants under normal conditions. It indicated that AOX pathway could influence chloroplast energy metabolism. Drought reduced carbon assimilation. Photoinhibition was caused by excess of absorbed light energy in spite of the increase of thermal energy dissipation and cyclic electron flow around PSI (CEF-PSI). Upregulation of AOX pathway in leaves experiencing drought would play a critical role in protection against photoinhibition by optimization of carbon assimilation and PSII function, which would avoid over-reduction of photosynthetic electron transport chain. However, inhibition of AOX pathway could be compensated by increasing the thermal energy dissipation and CEF-PSI under drought stress, and the compensation of CEF-PSI was especially significant.

Keywords: alternative oxidase pathway; Capsicum annuum L; chlorophyll fluorescence; drought; photoinhibition; photosynthesis

Received: September 30, 2017; Accepted: February 7, 2018; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Hu, W.H., Yan, X.H., He, Y., & Ye, X.L. (2018). Role of alternative oxidase pathway in protection against drought-induced photoinhibition in pepper leaves. Photosynthetica, 56(4), 1297-1303. doi: 10.1007/s11099-018-0837-1.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Allakhverdiev S.I.: Recent progress in the studies of structure and function of photosystem II.-J. Photoch. Photobio. B 104: 1-8, 2011. Go to original source...
    2. Allakhverdiev S.I., Klimov V.V., Carpentier R.: Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound.-Biochemistry 36: 4149-4154, 1997. Go to original source...
    3. Asada K.: The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.-Annu. Rev. Plant Biol. 50: 601-639, 1999. Go to original source...
    4. Bartoli C.G., Gomez F., Gergoff G. et al.: Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions.-J. Exp. Bot. 56: 1269-1276, 2005. Go to original source...
    5. Boyer J.S.: Plant productivity and environment.-Science 218: 443-448, 1982. Go to original source...
    6. Clifton R., Lister R., Parker K.L. et al.: Stress-induced coexpression of alternative respiratory chain components in Arabidopsis thaliana.-Plant Mol. Biol. 58: 193-212, 2005. Go to original source...
    7. Dahal K., Martyn G.D., Vanlerberghe G.C.: Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink.-New Phytol. 208: 382-395, 2015. Go to original source...
    8. Dahal K., Wang J., Martyn G.D. et al.: Mitochondrial alternative oxidase maintains respiration and preserves photosynthetic capacity during moderate drought in Nicotiana tabacum.-Plant Physiol. 166: 1560-1574, 2014. Go to original source...
    9. Demmig-Adams B., Adams III.W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis.-Trends Plant Sci. 1: 21-26, 1996. Go to original source...
    10. Eichelmann H., Talts E., Oja V. et al.: Rubisco in planta kcat is regulated in balance with photosynthetic electron transport.-J. Exp. Bot. 60: 4077-4088, 2009. Go to original source...
    11. Erice G., Louahlia S., Irigoyen J.J. et al.: Water use efficiency, transpiration and net CO2 exchange of four alfalfa genotypes submitted to progressive drought and subsequent recovery.-Environ. Exp. Bot. 72: 123-130, 2011. Go to original source...
    12. Feng H.Q., Tang S.Z., Sun K. et al.: Cyanide-resistant respiratory pathway is involved in the high-light systemic acquired acclimation of kidney bean (Phaseolus vulgaris).-Photosynthetica 53: 195-200, 2015. Go to original source...
    13. Foyer C.H., Vanacker H., Gomez L.D. et al.: Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review.-Plant Physiol. Bioch. 40: 659-668, 2002. Go to original source...
    14. Gandin A., Duffes C., Day D.A. et al.: The absence of alternative oxidase AOX1a results in altered response of photosynthetic carbon assimilation to increasing CO2 in Arabidopsis thaliana.-Plant Cell Physiol. 53: 1627-1637, 2012. Go to original source...
    15. Golding A.J., Johnson G.N.: Down-regulation of linear and activation of cyclic electron transport during drought.-Planta 218: 107-114, 2003. Go to original source...
    16. Govindjee, Wasielewski M.R.: Photosystem II: from a femtosecond to a millisecond.-In: Briggs W.R. (ed.): Photosynthesis. Pp. 71-103. Alan R. Liss, New York 1989.
    17. Hu W.H., Xiao Y.A., Zeng J.J. et al.: Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses.-Biol. Plantarum 54: 761-765, 2010. Go to original source...
    18. Hu W.H., Yan X.H. Yu J.Q.: Importance of the mitochondrial alternative oxidase (AOX) pathway in alleviating photoinhibition in cucumber leaves under chilling injury and subsequent recovery when leaves are subjected to high light intensity.-J. Hort. Sci. Biotech. 92: 31-38, 2017. Go to original source...
    19. Ivanov A.G., Hurry V., Sane P.V. et al.: Reaction centre quenching of excess light energy and photoprotection of photosystem II.-J. Plant Biol. 51: 85-96, 2008. Go to original source...
    20. Jia H., Oguchi R., Hope A.B. et al.: Differential effects of severe water stress on linear and cyclic electron fluxes through photosystem I in spinach leaf discs in CO2-enriched air.-Planta 228: 803-812, 2008. Go to original source...
    21. Lei Y., Zheng Y., Dai K. et al.: Different responses of photosystem I and photosystem II in three tropical oilseed crops exposed to chilling stress and subsequent recovery.-Trees 28: 923-933, 2014. Go to original source...
    22. Mamedov M., Govindjee, Nadtochenko V. et al.: Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms.-Photosynth. Res. 125: 51-63, 2015. Go to original source...
    23. Maxwell K., Johnson G.N.: Chlorophyll fluorescence-a practical guide.-J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    24. McKenzie S., McIntosh L.: Higher plant mitochondria.-Plant Cell 11: 571-585, 1999. Go to original source...
    25. Mohanty P., Allakhverdiev S.I., Murata N.: Application of low temperatures during photoinhibition allow characterization of individual steps in photodamage and the repair of photosystem II.-Photosynth. Res. 94: 217-224, 2007 Go to original source...
    26. Nunes-Nesi A., Sulpice R., Gibon Y. et al.: The enigmatic contribution of mitochondrial function in photosynthesis.-J. Exp. Bot. 59: 1675-1684, 2008.
    27. Ort D.R., Baker N.R.: A photoprotective for O2 as an alternative electron sink in photosynthesis.-Curr. Opin. Plant Biol. 5: 193-198, 2002.
    28. Padmasree K., Padmavathi L., Raghavendra A.S.: Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition.-Crit. Rev. Biochem. Mol. Biol. 37: 71-119, 2002. Go to original source...
    29. Raghavendra A.S., Padmasree K.: Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation.-Trends Plant Sci. 8: 546-553, 2003. Go to original source...
    30. Song X.S., Shang Z.W., Yin Z.P. et al.: Mechanism of xanthophyll-cycle-mediated photoprotection in Cerasus humilis seedlings under water stress and subsequent recovery.-Photosynthetica 49: 523-530, 2011. Go to original source...
    31. Taylor N.L., Day D.A., Millar A.H.: Environmental stress causes oxidative damage to plant mitochondrial leading to inhibition to glycine decarboxylase.-J. Biol. Chem. 277: 42663-42668, 2002. Go to original source...
    32. Tikkanen M., Mekala N.R., Aro E.M.: Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage.-BBA-Bioenergetics 1837: 210-215, 2014.
    33. Wagner A.M., Krab K.: The alternative respiration pathway in plants: role and regulation.-Physiol. Plant. 95: 318-325, 1995. Go to original source...
    34. Walker B.J., Strand D.D., Kramer D.M. et al.: The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation.-Plant Physiol. 165: 453-462, 2014. Go to original source...
    35. Yamori W., Sakata N., Suzuki Y. et al.: Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice.-Plant J. 68: 966-976, 2011. Go to original source...
    36. Ye Z.P.: A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa.-Photosynthetica 45: 637-640, 2007. Go to original source...
    37. Yin C.Y., Peng Y.H., Zang R.G. et al.: Adaptive responses of Populus kangdingensis to drought stress.-Physiol. Plantarum 123: 445-451, 2005. Go to original source...
    38. Yoshida K., Terashima I., Noguchi K.: Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis.-Plant Cell Physiol. 47: 22-31, 2006. Go to original source...
    39. Yoshida K., Terashima I., Noguchi K.: Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light.-Plant Cell Physiol. 48: 606-614, 2007. Go to original source...
    40. Yu J.Q., Matsui Y.: Effects of root exudates and allelochemical on ion uptake by cucumber seedlings.-J. Chem. Ecol. 23: 817-827, 1997. Go to original source...
    41. Zandalinas S.I., Rivero R.M., Martínez V. et al.: Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels.-BMC Plant Biol. 16: 105, 2016. Go to original source...
    42. Zhang L.T., Zhang Z.S., Gao H.Y. et al.: The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves.-BMC Plant Biol. 12: 40, 2012. Go to original source...
    43. Zhang L.T., Zhang Z.S., Gao H.Y. et al.: 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. Plantarum 143: 396-407, 2011. Go to original source...
    44. Živcák M., Brestic M., Balatova Z. et al.: Photosynthetic electron transport and specific photoprotective response in wheat leaves under drought stress.-Photosynth. Res. 117: 529-546, 2013. Go to original source...

    Return to the content