Photosynthetica 2017, 55(4):664-670 | DOI: 10.1007/s11099-016-0681-0

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

R. L. Xue1,2, S. Q. Wang2, H. L. Xu2, P. J. Zhang2, H. Li3, H. J. Zhao2,3,*
1 College of Agronomy, Henan Agricultural University, Zhengzhou, China
2 College of Life Sciences, Henan Agricultural University, Zhengzhou, China
3 State Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, China

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.

Keywords: antioxidant enzymes; cellular damage; high temperature; photosynthetic efficiency

Received: August 15, 2016; Accepted: October 27, 2016; Published: December 1, 2017Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Xue, R.L., Wang, S.Q., Xu, H.L., Zhang, P.J., Li, H., & Zhao, H.J. (2017). Progesterone increases photochemical efficiency of photosystem II in wheat under heat stress by facilitating D1 protein phosphorylation. Photosynthetica55(4), 664-670. doi: 10.1007/s11099-016-0681-0.
Download citation

References

  1. Aro E. M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
  2. Barber J., Andersson B.: Too much of a good thing: light can be bad for photosynthesis. - Trends Biochem. Sci. 17: 61-66, 1992. Go to original source...
  3. Beauchamp C., Fridovich I.: Superoxide dismutase:improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276-287, 1971. Go to original source...
  4. Bellafiore S., Barneche F., Peltier G., Rochaix JD.: State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. - Nature 433: 892-895, 2005. Go to original source...
  5. Berry J., Björkman O.: Photosynthetic response and adaptation to temperature in higher plants. - Annu. Rev. Plant Physio. 31: 491-543, 1980. Go to original source...
  6. Bowler C., Montagu M.V., Inze D.: Superoxide dismutase and stress tolerance. - Annu. Rev. Plant Phys. 43: 83-116, 1992. Go to original source...
  7. 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.
  8. 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. Go to original source...
  9. 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.
  10. Dogra R., Thukral A.K.: New Trends in Plant Physiology. Pp. 65-70. Today and Tomorrow's Printers and Publishers, New Delhi. 1991.
  11. 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. Go to original source...
  12. Erdal S.: Alleviation of salt stress in wheat seedlings by mammalian sex hormones. - J. Sci. Food Agr. 92: 1411-1416, 2012. Go to original source...
  13. Erdal S., Dumlupinar R.: Mammalian sex hormones stimulate antioxidant system and enhance growth of chickpea plants. - Acta Physiol. Plant. 33: 1011-1017, 2011. Go to original source...
  14. 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. Go to original source...
  15. Geuns J.M.C.: Steroid hormones and plant growth and development. - Phytochemistry 17: 1-14, 1978 Go to original source...
  16. 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]
  17. Havir E.A., McHale N.A.: Biochemical and development characterization of multiple forms of catalase in tobacco leaves. - Plant Physiol. 84: 450-455, 1987. Go to original source...
  18. Heath R.L., Packer L.: Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation.-Arch. Biochem. Biophys. 125: 189-198, 1968. Go to original source...
  19. Helmkamp G., Bonner J.: Some relationships of sterols to plant growth.-Plant Physiol. 28: 428-436, 1953. Go to original source...
  20. Jana S., Chaudhuri M.A.: Glycolate metabolism of three submerged aquatic angiosperms during aging. - Aquat. Bot. 12: 345-354, 1981. Go to original source...
  21. 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. Go to original source...
  22. 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. Go to original source...
  23. 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. Go to original source...
  24. 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. Go to original source...
  25. 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.
  26. 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. Go to original source...
  27. 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.
  28. Mittler R.: Abiotic stress, the field environment and stress combination. - Trend Plant Sci. 11: 15-19, 2006. Go to original source...
  29. 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. Go to original source...
  30. 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. Go to original source...
  31. Niyogi K.K.: Photoprotection revisited: genetic and molecular approaches. - Annu. Rev. Plant Phys. 50: 333-359, 1999. Go to original source...
  32. 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. Go to original source...
  33. 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.
  34. Powles S.B.: Photoinhibition of photosynthesis induced by visible light. - Annu. Rev. Plant Physio. 35: 15-44, 1984. Go to original source...
  35. 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. Go to original source...
  36. 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. Go to original source...
  37. 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. Go to original source...
  38. 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. Go to original source...
  39. 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. Go to original source...
  40. 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. Go to original source...
  41. 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. Go to original source...
  42. Wahid A., Gelani S., Ashraf M., Foolad M.R.: Heat tolerance in plants:an overview. - Environ. Exp. Bot. 61: 199-223, 2007. Go to original source...
  43. Yamamoto Y.: Quality control of photosystem II. - Plant Cell Physiol. 42: 121-128, 2001. Go to original source...
  44. 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. Go to original source...
  45. 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. Go to original source...
  46. 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. Go to original source...
  47. 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. Go to original source...