Photosynthetica, 2020 (vol. 58), 1

Photosynthetica 2020, 58(1):87-99 | DOI: 10.32615/ps.2019.156

Different responses of photosystem and antioxidant defense system to three environmental stresses in wheat seedlings

N. WU1, H.T. MAO1, M.Y. CHEN1, J. DONG1, M. YUAN1, Z.W. ZHANG2, S. YUAN2, H.Y. ZHANG1, Y.E. CHEN1
1 College of Life Sciences, Sichuan Agricultural University, 625014 Ya&5xA78C;an, China
2 College of Resources Science and Technology, Sichuan Agricultural University, 611130 Chengdu, China

To investigate the adaptive mechanism of wheat under high light, osmotic stress, and salt stress, redox regulation, and photosynthesis were compared. Under high light, the activities of antioxidant enzymes, except for catalase, significantly increased and then decreased after 1 and 3 h, respectively. Under osmotic stress, antioxidant enzyme activities significantly increased and subsequently declined. Except for superoxide dismutase, salt stress induced a significant increase in all the antioxidant enzyme activities. A significant decrease of D1 protein by high light and osmotic stress, strong photophosphorylation of D1 and D2 under high light and salt stress were observed, while all the stresses induced upregulation of PsbS protein. Eight stress-associated genes (TaMYB73, TaABC1, TaOPR1, TaASR1, TaWRKY44, TaWRKY2, TaWRKY19, and TaCIPK29) showed different expression levels under all the stresses. We conclude that the wheat plant adopted various strategies by regulating the antioxidant system, expression of stress-responsive genes, and photosystems under different abiotic stresses.

Keywords: chlorophyll fluorescence; gene expression; reactive oxygen species; Triticum aestivum.

Received: August 25, 2019; Accepted: November 18, 2019; Prepublished online: December 20, 2019; Published: March 10, 2020Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
WU, N., MAO, H.T., CHEN, M.Y., DONG, J., YUAN, M., ZHANG, Z.W., ... CHEN, Y.E. (2020). Different responses of photosystem and antioxidant defense system to three environmental stresses in wheat seedlings. Photosynthetica58(1), 87-99. doi: 10.32615/ps.2019.156.
Download citation

Supplementary files

Download fileWu 2369 supplement.doc

File size: 6.66 MB

References

  1. Adir N., Zer H., Shochat S., Ohad I.: Photoinhibition - a historical perspective. - Photosynth. Res. 76: 343-370, 2003. Go to original source...
  2. Allen J.F.: Protein phosphorylation in regulation of photo-synthesis. - BBA-Bioenergetics 1098: 275-335, 1992. Go to original source...
  3. Arnon D.I.: Copper enzymes in isolated chloroplasts. Polyphenol-oxidase in Beta vulgaris. - Plant Physiol. 24: 267-272, 1949. Go to original source...
  4. Baker N.R.: Chlorophyll fluorescence: a probe of photosynthesis in vivo. - Annu. Rev. Plant Biol. 59: 89-113, 2008. Go to original source...
  5. Barnabás B., Jäger K., Fehér A.: The effect of drought and heat stress on reproductive processes in cereals. - Plant Cell Environ. 31: 11-38, 2008.
  6. Bartoli C.G., Simontacchi M., Tambussi E. et al.: Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. - J. Exp. Bot. 50: 375-383, 1999. Go to original source...
  7. Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
  8. Bechtold U., Murphy D.J., Mullineaux P.M.: Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. - Plant Cell 16: 908-919, 2004. Go to original source...
  9. Beers Jr. R.F., Sizer I.W.: A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. - J. Biol. Chem. 195: 133-140, 1952.
  10. Bowne J.B., Erwin T.A., Juttner J. et al.: Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. - Mol. Plant 5: 418-429, 2012. Go to original source...
  11. Boyer J.S.: Plant productivity and environment. - Science 218: 443-448, 1982. Go to original source...
  12. Chaitanya K.V., Sundar D., Masilamani S., Reddy A.R.: Variation in heat stress-induced antioxidant enzyme activities among three mulberry cultivars. - Plant Growth Regul. 36: 175-180, 2002. Go to original source...
  13. Chaves M.M.: Effects of water deficits on carbon assimilation. - J. Exp. Bot. 42: 1-16, 1991. Go to original source...
  14. Chen X.Y., Li W., Lu Q.T. et al.: The xanthophyll cycle and antioxidative defense system are enhanced in the wheat hybrid subjected to high light stress. - J. Plant Physiol. 168: 1828-1836, 2011.
  15. Chen Y.E., Cui J.M., Su Y.Q. et al.: Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. - Front. Plant Sci. 6: 779, 2015. Go to original source...
  16. Chen Y.E., Liu W.J., Su Y.Q. et al.: Different response of photo-system II to short and long-term drought stress in Arabidopsis thaliana. - Physiol. Plantarum 158: 225-235, 2016a. Go to original source...
  17. Chen Y.E., Mao J.J., Sun L.Q. et al.: Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. - Physiol. Plantarum 164: 349-363, 2018. Go to original source...
  18. Chen Y.E., Yuan S., Schröder W.P.: Comparison of methods for extracting thylakoid membranes of Arabidopsis plants. - Physiol. Plantarum 156: 3-12, 2016b. Go to original source...
  19. Chen Y.E., Zhang C.M., Su Y.Q. et al.: Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat. - Environ. Exp. Bot. 135: 45-55, 2017. Go to original source...
  20. Cossani C.M., Reynolds M.P.: Physiological traits for improving heat tolerance in wheat. - Plant Physiol. 160: 1710-1718, 2012. Go to original source...
  21. de Bianchi S., Betterle N., Kouril R. et al.: Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. - Plant Cell 23: 2659-2679, 2011. Go to original source...
  22. de Bianchi S., Dall'Osto L., Tognon G. et al.: Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. - Plant Cell 20: 1012-1028, 2008. Go to original source...
  23. Deng X., Hu W., Wei S. et al.: TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. - PLoS ONE 8: e69881, 2013. Go to original source...
  24. Dong W., Wang M., Xu F. et al.: Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. - Plant Physiol. 161: 1217-1228, 2013. Go to original source...
  25. Farooq M., Bramley H., Palta J.A. et al.: Heat stress in wheat during reproductive and grain-filling phases. - Crit. Rev. Plant Sci. 30: 491-507, 2011. Go to original source...
  26. Flowers T.J.: Improving crop salt tolerance. - J. Exp. Bot. 55: 307-319, 2004. Go to original source...
  27. Foyer C.H., Halliwell B.: The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. - Planta 133: 21-25, 1976. Go to original source...
  28. Fristedt R., Willig A., Granath P. et al.: Phosphorylation of photosystem II controls functional macroscopic folding of plant photosynthetic membranes in Arabidopsis. - Plant Cell 21: 3950-3964, 2009. Go to original source...
  29. Giannopolitis C.N., Ries S.K.: Superoxide dismutases: I. Occur-rence in higher plants. - Plant Physiol. 59: 309-314, 1977. Go to original source...
  30. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
  31. Gilmore A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplast and leaves. - Physiol. Plantarum 99: 197-209, 1997. Go to original source...
  32. Grassi G., Magnani F.: Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. - Plant Cell Environ. 28: 834-849, 2005. Go to original source...
  33. Havir E.A., McHale N.A.: Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. - Plant Physiol. 84: 450-455, 1987. Go to original source...
  34. He Y., Li W., Lv J. et al.: Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. - J. Exp. Bot. 63: 1511-1522, 2012. Go to original source...
  35. Hu W., Huang C., Deng X. et al.: TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. - Plant Cell Environ. 36: 1449-1464, 2013. Go to original source...
  36. James R.A., von Caemmerer S., Condon A.G. (Tony) et al.: Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. - Funct. Plant Biol. 35: 111-123, 2008. Go to original source...
  37. Klughammer C., Schreiber U.: An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. - Planta 192: 261-268, 1994. Go to original source...
  38. Kovács L., Damkjær J., Kereïche S. et al.: Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. - Plant Cell 18: 3106-3120, 2006. Go to original source...
  39. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. -Methods 25: 402-408, 2001. Go to original source...
  40. Loggini B., Scartazza A., Brugnoli E., Navari-Izzo F.: Anti-oxidative defense system, pigment composition, and photo-synthetic efficiency in two wheat cultivars subjected to drought. - Plant Physiol. 119: 1091-1099, 1999. Go to original source...
  41. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J.: Protein measurement with the Folin phenol reagent. - J. Biol. Chem. 193: 265-275, 1951.
  42. Maxwell K., Johnson G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
  43. Mbarki S., Sytar O., Živčák M. et al.: Anthocyanins of coloured wheat genotypes in specific response to salt stress. - Molecules 23: 1518, 2018. Go to original source...
  44. Mehler A.H.: Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. - Arch. Biochem. Biophys. 34: 339-351, 1951. Go to original source...
  45. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F.: Reactive oxygen gene network of plants. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
  46. Mittler R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  47. Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I.: Photoinhibition of photosystem II under environmental stress. -BBA-Bioenergetics 1767: 414-421, 2007. Go to original source...
  48. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
  49. Niu C.F., Wei W., Zhou Q.Y. et al.: Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. - Plant Cell Environ. 35: 1156-1170, 2012. Go to original source...
  50. Niyogi K.K.: Safety valves for photosynthesis. - Curr. Opin. Plant Biol. 3: 455-460, 2000. Go to original source...
  51. Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control. - Annu. Rev. Plant Phys. 49: 249-279, 1998. Go to original source...
  52. Okuda T., Matsuda Y., Yamanaka A., Sagisaka S.: Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. - Plant Physiol. 97: 1265-1267, 1991. Go to original source...
  53. Pietrzykowska M., Suorsa M., Semchonok D.A. et al.: The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. - Plant Cell 26: 3646-3660, 2014. Go to original source...
  54. Porra R.J., Thompson W.A., Kriedemann P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. - BBA-Bioenergetics 975: 384-394, 1989. Go to original source...
  55. Powles S.B.: Photoinhibition of photosynthesis induced by visible light. - Ann. Rev. Plant Physio. 35: 15-44, 1984. Go to original source...
  56. Ramakrishna A., Ravishankar G.A.: Influence of abiotic stress signals on secondary metabolites in plants. - Plant Signal. Behav. 6: 1720-1731, 2011.
  57. Ranjbarfordoei A., Samson R., Lemeur R., Van Damme P.: Effects of osmotic drought stress induced by a combination of NaCl and polyethylene glycol on leaf water status, photosynthetic gas exchange, and water use efficiency of Pistacia khinjuk and P. mutica. - Photosynthetica 40: 165-169, 2002. Go to original source...
  58. Rico C.M., Hong J., Morales M.I. et al.: Effect of cerium oxide nanoparticles on rice: a study involving the antioxidant defense system and in vivo fluorescence imaging. - Environ. Sci. Technol. 47: 5635-5642, 2013. Go to original source...
  59. Rizhsky L., Liang H.J., Shuman J. et al.: When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. - Plant Physiol. 134: 1683-1696, 2004. Go to original source...
  60. Shah F., Huang J., Cui K. et al.: Impact of high-temperature stress on rice plant and its traits related to tolerance. - J. Agr. Sci. 149: 545-556, 2011. Go to original source...
  61. Singh A.K., Singhal G.S.: Effect of irradiance on the thermal stability of thylakoid membrane isolated from acclimated wheat leaves. - Photosynthetica 39: 23-27, 2001. Go to original source...
  62. Smirnoff N.: The role of active oxygen in the response of plants to water deficit and desiccation. - New Phytol. 125: 27-58, 1993. Go to original source...
  63. Sonoike K.: Photoinhibition of photosystem I. - Physiol. Plantarum 142: 56-64, 2011. Go to original source...
  64. Sperdouli I., Moustakas M.: Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. - J. Plant Physiol. 169: 577-585, 2012. Go to original source...
  65. Sytar O., Živčák M., Brücková K. et al.: Shift in accumulation of flavonoids and phenolic acids in lettuce attributable to changes in ultraviolet radiation and temperature. - Sci. Hortic.-Amsterdam 239: 193-204, 2018.
  66. Thomas T.A.: An automated procedure for the determination of soluble carbohydrates in herbage. - J. Sci. Food Agr. 28: 639-642, 1977. Go to original source...
  67. Tikkanen M., Aro E.M.: Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. - BBA-Bioenergetics 1817: 232-238, 2012.
  68. van Wees S.: Phenotypic analysis of Arabidopsis mutants: trypan blue stain for fungi, oomycetes, and dead plant cells. - CSH Protoc. 3: pdb.prot4982, 2008.
  69. Verma S., Mishra S.N.: Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. - J. Plant Physiol. 162: 669-677, 2005. Go to original source...
  70. Wang C., Jing R., Mao X. et al.: TaABC1, a member of the activity of bc1 complex protein kinase family from common wheat, confers enhanced tolerance to abiotic stresses in Arabidopsis. -J. Exp. Bot. 62: 1299-1311, 2011. Go to original source...
  71. Wang X., Zeng J., Li Y. et al.: Expression of TaWRKY44, a wheat WRKY gene, in transgenic tobacco confers multiple abiotic stress tolerances. - Front. Plant Sci. 6: 615, 2015. Go to original source...
  72. Ware M.A., Belgio E., Ruban A.V.: Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. - J. Exp. Bot. 66: 1259-1270, 2014.
  73. Xu C.P., Huang, B. R.: Differential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars differing in stress tolerance. - J. Plant Physiol. 167: 1477-1485, 2010. Go to original source...
  74. Xu J., Zhu Y.Y., Ge Q. et al.: Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. - New Phytol. 196: 125-138, 2012. Go to original source...
  75. Zhang H.J., Zhang N., Yang R.C. et al.: Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). - J. Pineal Res. 57: 269-279, 2014. Go to original source...
  76. Zhang W.E., Wang F., Pan X.J. et al.: Antioxidant enzymes and photosynthetic responses to drought stress of three Canna edulis cultivars. - Korean J. Hortic. Sci. 31: 677-686, 2013.
  77. Zhang Z., Chen J., Su Y. et al.: TaLHY, a 1R-MYB transcription factor, plays an important role in disease resistance against stripe rust fungus and ear heading in wheat. - PLoS ONE 10: e0127723, 2015. Go to original source...