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Progesterone increases photochemical efficiency of photosystem II in wheat under heat stress by facilitating D1 protein phosphorylation

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Photosynthetica

Abstract

Experiments were conducted to investigate the effects of exogenous progesterone on photochemical efficiency of PSII and turnover of D1 protein under heat stress during the grain-filling stage. Heat stress resulted in increases of hydrogen peroxide production, malondialdehyde content, and relative electrolytic leakage in wheat leaves, but these responses were alleviated by foliar application of progesterone. Meanwhile, activities of superoxide dismutase, catalase, and peroxidase were significantly improved in progesterone-pretreated leaves. Along with the alleviation of oxidative stress, higher abundances of STN8 and phosphorylated D1 protein and lower total D1 protein content in the PSII reactive center were observed in progesterone-pretreated leaves relative to controls. Consequently, progesterone raised the potential photochemical efficiency, actual photochemical efficiency, and electron transfer rate. These results indicate that foliar application of progesterone can effectively alleviate heat-induced PSII damage by enhancing antioxidant capability and regulating phosphorylation of D1 protein in wheat leaves.

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Abbreviations

CAT:

catalase

Chl:

chlorophyll

ETR:

electron transfer rate

Fo :

minimal fluorescence yield of the dark-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

Fm':

maximal fluorescence yield of the light-adapted state

Ft :

steady-state fluorescence

Fv :

variable fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

MDA:

malondialdehyde

MSH:

mammalian sex hormone

POD:

peroxidase

REC:

relative electrical conductivity

ROS:

reactive oxygen species

SDS:

sodium dodecyl sulfate

SOD:

superoxide dismutase

ФPSII :

effective quantum yield of PSII photochemistry

References

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

    Article  CAS  PubMed  Google Scholar 

  • Barber J., Andersson B.: Too much of a good thing: light can be bad for photosynthesis. — Trends Biochem. Sci. 17: 61–66, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C., Fridovich I.: Superoxide dismutase:improved assays and an assay applicable to acrylamide gels. — Anal. Biochem. 44: 276–287, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Bellafiore S., Barneche F., Peltier G., Rochaix JD.: State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. — Nature 433: 892–895, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Berry J., Björkman O.: Photosynthetic response and adaptation to temperature in higher plants. — Annu. Rev. Plant Physio. 31: 491–543, 1980.

    Article  Google Scholar 

  • Bowler C., Montagu M.V., Inze D.: Superoxide dismutase and stress tolerance. — Annu. Rev. Plant Phys. 43: 83–116, 1992.

    Article  CAS  Google Scholar 

  • Callahan F. E., Ghirardi M.L., Sopory S. K. et al.: A novel metabolic form of the 32 kDa-D1 protein in the grana-localized reaction center of photosystem II. — J. Biol. Chem. 265: 15357–15360, 1990.

    CAS  PubMed  Google Scholar 

  • Depège N., Bellafiore S., Rochaix J.D.: Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. — Science 299: 1572–1575, 2003.

    Article  PubMed  Google Scholar 

  • Dogra R., Kaur A.: Effect of steroids on some growth and biochemical parameters of Triticum aestivum L. during germination. — Crop Res. 8: 611–620, 1994.

    Google Scholar 

  • Dogra R., Thukral A.K.: New Trends in Plant Physiology. Pp. 65–70. Today and Tomorrow's Printers and Publishers, New Delhi. 1991.

    Google Scholar 

  • Enami I., Kitamura M., Tomo T. et al.: Is the primary cause of thermal inactivation of oxygen evolution in spinach PSII membranes release of the extrinsic 33 kDa protein or of Mn? — Biochim. Biophys. Acta 1186: 52–58, 1994.

    Article  CAS  Google Scholar 

  • Erdal S.: Alleviation of salt stress in wheat seedlings by mammalian sex hormones. — J. Sci. Food Agr. 92: 1411–1416, 2012.

    Article  CAS  Google Scholar 

  • Erdal S., Dumlupinar R.: Mammalian sex hormones stimulate antioxidant system and enhance growth of chickpea plants. — Acta Physiol. Plant. 33: 1011–1017, 2011.

    Article  CAS  Google Scholar 

  • Foyer C. H., Lopez-Delgado H., Dat J. F. et al.: Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. — Physiol. Plantarum 100: 241–254, 1997.

    Article  CAS  Google Scholar 

  • Geuns J.M.C.: Steroid hormones and plant growth and development. — Phytochemistry 17: 1–14, 1978

    Article  CAS  Google Scholar 

  • Guo J.W., Wei H.M., Wu S. F., Du L.F.: [Effects of low temperature on the distribution of excitation energy in photosystem and the phosphorylation of thylakoid membrane proteins in rice.]. — Acta Biophys. Sin. 22: 197–202, 2006. [In Chinese]

    CAS  Google Scholar 

  • Havir E.A., McHale N.A.: Biochemical and development characterization of multiple forms of catalase in tobacco leaves. — Plant Physiol. 84: 450–455, 1987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heath R.L., Packer L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation.–Arch. Biochem. Biophys. 125: 189–198, 1968.

    Article  CAS  PubMed  Google Scholar 

  • Helmkamp G., Bonner J.: Some relationships of sterols to plant growth.–Plant Physiol. 28: 428–436, 1953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jana S., Chaudhuri M.A.: Glycolate metabolism of three submerged aquatic angiosperms during aging. — Aquat. Bot. 12: 345–354, 1981.

    Article  Google Scholar 

  • Janeczko A., Oklešťková J., Siwek A. et al.: Endogenous progesterone and its cellular binding sites in wheat exposed to drought stress. — J. Steroid Biochem. 138: 384–394, 2013.

    Article  CAS  Google Scholar 

  • Janeczko A., Koscielniak J., Pilipowicz M. et al.: Protection of winter rape photosystem II by 24-epibrassinolide under cadmium stress. — Photosynthetica 43: 293–298, 2005.

    Article  CAS  Google Scholar 

  • Janeczko A., Tóbiás I., Skoczowski A. et al.: Progesterone moderates damage in Arabidopsis thaliana caused by infection with Pseudomonas syringae or P. fluorescens. — Biol. Plantarum 57: 169–173, 2013.

    Article  CAS  Google Scholar 

  • Jiang Y.W., Huang B.R.: Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation. — Crop Sci. 41: 436–442, 2001.

    Article  CAS  Google Scholar 

  • Kato Y., Miura E., Ido K. et al.: The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. — Plant Physiol. 151: 1790–1801, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato Y., Sakamoto W.: Phosphorylation of photosystem II core proteins prevents undesirable cleavage of D1 and contributes to the fine-tuned repair of photosystem II. — Plant J. 79: 312–321, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Li H.S., Sun Q., Zhao S.J.: Principle and Technology of Plant Physiology and Biochemical Experiments. Pp. 261–263. Higher Educ. Press, Beijing 2000.

    Google Scholar 

  • Mittler R.: Abiotic stress, the field environment and stress combination. — Trend Plant Sci. 11: 15–19, 2006.

    Article  CAS  Google Scholar 

  • Nash D., Mitsue M., Murata N.: Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. — BBABioenergetics 807: 127133, 1985.

    Google Scholar 

  • Nath K., Poudyal R.S., Eom J.S., Park Y.S. et al.: Loss-offunction of OsSTN8 suppresses the photosystem II core protein phosphorylation and interferes with the photosystem II repair mechanism in rice (Oryza sativa). — Plant J. 76: 675–686, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Niyogi K.K.: Photoprotection revisited: genetic and molecular approaches. — Annu. Rev. Plant Phys. 50: 333–359, 1999.

    Article  CAS  Google Scholar 

  • Obinger C., Maj M., Nicholls P., Loewen P.: Activity, peroxide compound formation, and heme d synthesis in Escherichia coli HPII catalase. — Arch. Biochem. Biophys. 342: 58–67, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Pesaresi P., Pribil M., Wunder T., Leister D.: Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. — Biochim. Biophys. Acta 1807: 887–896, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Powles S.B.: Photoinhibition of photosynthesis induced by visible light. — Annu. Rev. Plant Physio. 35: 15–44, 1984.

    Article  CAS  Google Scholar 

  • Rainwater D.T., Gossett D.R., Millhollon E.P. et al.: The relationship between yield and the antioxidant defence system in tomatoes grown under heat stress. — Free Radical Res. 25: 421–435, 1996.

    Article  CAS  Google Scholar 

  • Samol I., Shapiguzov A., Ingelsson B. et al.: Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. — Plant Cell 24: 2596–2609, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A.K., Singhal G.S.: Effect of irradiance on the thermal stability of thylakoid membrane isolated from acclimated wheat leases. — Photosynthetica 39: 23–27, 2001.

    Article  CAS  Google Scholar 

  • Su X.Y., Wu S., Yang L. et al.: Exogenous progesterone alleviates heat and high light stress-induced inactivation of photosystem II in wheat by enhancing antioxidant defense and D1 protein stability. — Plant Growth Regul. 74: 311–318, 2014.

    Article  CAS  Google Scholar 

  • Tikkanen M., Nurmi M., Kanqasjärvi S., Aro E.M.: Core protein phosphorylation facilitates the respair of photodamaged photosystem II at high light. — Biochim. Biophys. Acta 1777: 14321437, 2008.

    Google Scholar 

  • Vacca R.A., de Pinto M.C., Valenti D. et al.: Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. — Plant Physiol. 134: 1100–1112, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vainonen J.P., Hansson M., Vener A.V.: STN8 Protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. — J. Biol. Chem. 280: 33679–33686, 2005.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Yamamoto Y.: Quality control of photosystem II. — Plant Cell Physiol. 42: 121–128, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y., Aminaka R., Yoshika M. et al.: Quality control of photosystem II: impact of light and heat stresses. — Photosynth. Res. 98: 589–608, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Yamashita A., Nijo N., Pospíšil P. et al.: 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, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X.H., Chen X.Y., Ge Q.Y. et al.: Tolerance of photosynthesis to photoinhibition, high temperature and drought stress in flag leaves of wheat: A comparison between a hybridization line and its parents grown under field conditions. — Plant Sci. 171: 389–397, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Zhao H.J., Zhao X.J., Ma P.F. et al.: Effects of salicylic acid on protein kinase activity and chloroplast D1 protein degradation in wheat leaves subjected to heat and high light stress. — Acta Ecol. Sin. 31: 259–263, 2011.

    Article  Google Scholar 

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Authors and Affiliations

  1. College of Agronomy, Henan Agricultural University, Zhengzhou, 450002, China

    R. L. Xue

  2. College of Life Sciences, Henan Agricultural University, Zhengzhou, 450002, China

    R. L. Xue, S. Q. Wang, H. L. Xu, P. J. Zhang & H. J. Zhao

  3. State Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, 450002, China

    H. Li & H. J. Zhao

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  1. R. L. Xue
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  2. S. Q. Wang
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  3. H. L. Xu
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  4. P. J. Zhang
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  5. H. Li
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  6. H. J. Zhao
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Correspondence to H. J. Zhao.

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Acknowledgements: This research was supported by the fund of the State Key Laboratory of Wheat and Maize Crop Science (SKL2014KF-06) and Agricultural Science and Technology Research Project of Henen Province, China (132102110125).

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Xue, R.L., Wang, S.Q., Xu, H.L. et al. Progesterone increases photochemical efficiency of photosystem II in wheat under heat stress by facilitating D1 protein phosphorylation. Photosynthetica 55, 664–670 (2017). https://doi.org/10.1007/s11099-016-0681-0

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  • DOI: https://doi.org/10.1007/s11099-016-0681-0

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