Photosynthetica 2018, 56(3):861-872 | DOI: 10.1007/s11099-017-0741-0

Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress

Y. Y. Guo1, S. S. Tian1, S. S. Liu1, W. Q. Wang1, N. Sui1,*
1 Shandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal University, Jinan, China

The effect of drought stress on energy dissipation and antioxidant enzyme system in two sweet sorghum inbred lines (M-81E and Roma) was investigated. Results showed that the germination indicator increased more in M-81E than that in Roma under rehydration. Under drought stress, both the maximal photochemical efficiency of PSII (Fv/Fm) and oxidoreductive activity (ΔI/I0) of Roma decreased more than those in M-81E. Relative to Fv/Fm, the ΔI/I0 decreased markedly, which indicated that PSI was more sensitive to drought stress than PSII. Increases in the reduction state of QA (1-qp), nonphotochemical quenching (NPQ) and minimal fluorescence yield of the dark-adapted state (F0) were greater in Roma than those in M-81E; meanwhile, the H2O2 content was lower in M-81E than that in Roma. Our results suggested that the photoinhibition might be related to the accumulation of reactive oxygen species (ROS). The antioxidant enzyme system and energy dissipation of M-81E could respectively increase drought tolerance by eliminating ROS and excess energy more efficiently than that of Roma.

Additional key words: antioxidant enzymes; chlorophyll fluorescence; environmental stress; sorghum bicolor; water

Received: June 2, 2016; Accepted: April 24, 2017; Prepublished online: September 1, 2018; Published: August 1, 2018Show citation

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Guo, Y.Y., Tian, S.S., Liu, S.S., Wang, W.Q., & Sui, N. (2018). Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica, 56(3), 861-872. doi: 10.1007/s11099-017-0741-0
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    References

    1. Agarie S., Hanaoka N., Ueno O. et al.: Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L.), monitored by electrolyte leakage.-Plant Prod. Sci. 1: 96-103, 1998. Go to original source...
    2. Ahmad S., Ahmad R., Ashraf M.Y. et al.: Sunflower (Helianthus annuus L.) response to drought stress at germination and seedling growth stages.-Pak. J. Bot. 41: 647-654, 2009.
    3. Ahmed C.B., Rouina B.B., Sensoy S. et al.: Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes.-Environ. Exp. Bot. 67: 345-352, 2009. Go to original source...
    4. Almodares A., Hadi M.R.: Production of bioethanol from sweet sorghum.-Afr. J. Agr. Res. 4: 772-780, 2009.
    5. Anjum S.A., Xie X., Wang L. et al.: Morphological, physiological and biochemical responses of plants to drought stress.-Afr. J. Agr. Res. 6: 2026-2032, 2011.
    6. Asada K.: Ascorbate peroxidase a hydrogen peroxide scavenging enzyme in plants.-Physiol. Plantarum 85: 235-241, 1992. Go to original source...
    7. 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...
    8. Ashraf M., Foolad M.: Roles of glycine betaine and proline in improving plant abiotic stress resistance.-Environ. Exp. Bot. 59: 206-216, 2007. Go to original source...
    9. Ashraf M., Harris P.J.C.: Photosynthesis under stressful environments: an overview.-Photosynthetica 51: 163-190, 2013. Go to original source...
    10. Awika J.M., Rooney L.W.: Sorghum phytochemicals and their potential impact on human health.-Phytochemistry 65: 1199-1221, 2004. Go to original source...
    11. Bacelar E.A., Santos D.L., Moutinho-Pereira J.M. et al.: Physiological behaviour, oxidative damage and antioxidative protection of olive trees grown under different irrigation regimes.-Plant Soil 292: 1-12, 2007. Go to original source...
    12. Bai Z.Y., Li C.D., Zhao J.F. et al.: Effect and preliminary analysis of chromosomal control on the chlorophyll fluorescence parameters of wheat substitution lines between synthetic hexaploid wheat and Chinese spring under drought stress.-Sci. Agric. Sin. 1: 7, 2011. [In Chinese]
    13. Baker N.R.: A possible role for photosystem II in environmental perturbations of photosynthesis.-Physiol. Plantarum 81: 563-570, 1991. Go to original source...
    14. Ballesteros M., Oliva J.M., Negro M.J. et al.: Ethanol from lignocellulosic materials by a simultaneous saccharification and fermentation process (SFS) with Kluyveromyces marxianus CECT 10875.-Process Biochem. 39: 1843-1848, 2004. Go to original source...
    15. Beiragi M.A., Ebrahimi M., Mostafavi K. et al.: A study of morphological basis of corn (Zea mays L.) yield under drought stress condition using correlation and path coefficient analysis.-J. Cereals Oilseeds 2: 32-37, 2011.
    16. Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976. Go to original source...
    17. Burnett S., Thomas P., van Iersel M.: Postgermination drenches with PEG-8000 reduce growth of salvia and marigolds.-HortScience 40: 675-679, 2005. Go to original source...
    18. Buschmann C., Konanz S., Zhou M. et al.: Excitation kinetics of chlorophyll fluorescence during light-induced greening and establishment of photosynthetic activity of barley seedlings.-Photosynthetica 51: 221-230, 2013. Go to original source...
    19. Cosentino S.L.: Crop physiology of sweet sorghum (Sorghum bicolor (L.) Moench).-In: Proceedings of First European Seminar on Sorghum for Energy and Industry. Pp. 1-3. 1996.
    20. Delachiave M.E.A., Pinho S.Z.: Germination of Senna occidentalis link: seed at different osmotic potential levels.-Braz. Arch. Biol. Techn. 46: 163-166, 2003. Go to original source...
    21. Dhanda S., Sethi G., Behl R.K.: Indices of drought tolerance in wheat genotypes at early stages of plant growth.-J. Agron. Crop Sci. 190: 6-12, 2004. Go to original source...
    22. Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A.: Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase.-J. Exp. Bot. 32: 93-101, 1981. Go to original source...
    23. El-Sharkawy M.A.: Prospects of photosynthetic research for increasing agricultural productivity, with emphasis on the tropical C4 Amaranthus and the cassava C3-C4 crops.-Photosynthetica 54: 161-184, 2016. Go to original source...
    24. Evans R., Skaggs R., Sneed R.: Normalized crop susceptibility factors for corn and soyabean to excess water stress.-T. ASAE 33: 1153-1161, 1990. Go to original source...
    25. Farsiani A., Ghobadi M.: Effects of PEG and NaCl stress on two cultivars of corn (Zea mays L.) at germination and early seedling stages.-World Acad. Sci. Eng. Tech. 57: 382-385, 2009.
    26. Foyer C.H., Lelandais M., Kunert K.J.: Photooxidative stress in plants.-Physiol. Plantarum 92: 696-717, 1994. Go to original source...
    27. Fridovich I.: Superoxide dismutases.-Annu. Rev. Bioch. 44: 147-159, 1975. Go to original source...
    28. Fu J., Huang B.: Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress.-Environ. Exp. Bot. 45: 105-114, 2001. Go to original source...
    29. Gill P.K., Sharma A.D., Singh P. et al.: Osmotic stress-induced changes in germination, growth and soluble sugar content of Sorghum bicolor (L.) Moench seeds.-Bulg. J. Plant Physiol. 28: 12-25, 2002.
    30. 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...
    31. Hamayun M., Sohn E.Y., Khan S.A. et al.: Silicon alleviates the adverse effects of salinity and drought stress on growth and endogenous plant growth hormones of soybean (Glycine max L.).-Pak. J. Bot. 42: 1713-1722, 2010.
    32. Havaux M., Strasser R.J., Greppin H.: A theoretical and experimental analysis of the qP and qn coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events.-Photosynth. Res. 27: 41-55, 1991. Go to original source...
    33. Horton P., Ruban A.V., Walters R.G.: Regulation of light harvesting in green plants (indication by nonphotochemical quenching of chlorophyll fluorescence).-Plant Physiol. 106: 415-420, 1994. Go to original source...
    34. Igartua E., Gracia M., Lasa J.: Field responses of grain sorghum to a salinity gradient.-Field Crop Res. 42: 15-25, 1995. Go to original source...
    35. Inoue K., Fujii T., Yokoyama E. et al.: The photoinhibition site of photosystem I in isolated chloroplasts under extremely reducing conditions.-Plant Cell Physiol. 30: 65-71, 1989. Go to original source...
    36. Jajarmi V.: Effect of water stress on germination indices in seven wheat cultivar.-World Acad. Sci. Eng. Technol. 49: 105-106, 2009.
    37. Jiménez C., Pick U.: Differential reactivity of [beta]-carotene isomers from Dunaliella bardawil toward oxygen radicals.-Plant Physiol. 101: 385-390, 1993. Go to original source...
    38. Jimenez L.D., Ayer W.A., Tewari J.P.: Phytoalexins produced in the leaves of Capsella bursa-pastoris (shepherd's purse).-Phytoprotection 78: 99-103, 1997. Go to original source...
    39. Jordan W., Dugas W., Shouse P.: Strategies for crop improvement for drought-prone regions.-Agr. Water Manage. 7: 281-299, 1983. Go to original source...
    40. Kanematsu S., Asada K.: Characteristic amino acid sequences of chloroplast and cytosol isozymes of CuZn superoxide dismutase in spinach, rice and horsetail.-Plant Cell Physiol. 31: 99-112, 1990.
    41. Khayatnezhad M., Gholamin R., Jamaati-e-Somarin S. et al.: Effects of peg stress on corn cultivars (Zea mays L.) at germination stage.-World Appl. Sci. J. 11: 504-506, 2010.
    42. Kozuleva M., Klenina I., Proskuryakov I. et al.: Production of superoxide in chloroplast thylakoid membranes: ESR study with cyclic hydroxylamines of different lipophilicity.-FEBS Lett. 585: 1067-1071, 2011. Go to original source...
    43. Kozuleva M.A., Petrova A.A., Mamedov M.D. et al.: O2 reduction by photosystem I involves phylloquinone under steady state illumination.-FEBS Lett. 588: 4364-4368, 2014. Go to original source...
    44. Lawlor, D.W.: The effects of water deficit on photosynthesis.-In: Smirnoff N. (ed.): Environment and Plant Metabolism. Flexibility and Acclimation. Pp. 129-160. BIOS Sci. Publ., Oxford 1995.
    45. Lei Y., Yin C., Li C.: Differences in some morphological, physiological, and biochemical responses to drought stress in two contrasting populations of Populus przewalskii.-Physiol. Plantarum 127: 182-191, 2006. Go to original source...
    46. Li X.G., Meng Q.W., Jiang G.Q., Zou Q.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle.-Photosynthetica 41: 259-265, 2003. Go to original source...
    47. Li Y.C., Fan W.G., Chen S.L.: Soil drought stress on membranelipid per-oxidation and antioxidant enzymes in pear rootstock.-J. Zhejiang Forestry Coll. 25: 437-441, 2008.
    48. Mehdy M.C.: Active oxygen species in plant defense against pathogens.-Plant Physiol. 105: 467-472, 1994. Go to original source...
    49. Mehler A.H.: Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents.-Arch. Biochem. Biophys. 33: 65-77, 1951. Go to original source...
    50. Miyake C., Asada K.: Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids.-Plant Cell Physiol. 33: 541-553, 1992.
    51. Mohammadkhani N., Heidari R.: Drought-induced accumulation of soluble sugars and proline in two maize varieties.-World Appl. Sci. J. 3: 448-453, 2008.
    52. Mubarakshina M.M., Ivanov B.N.: The production and scavenging of reactive oxygen species in the plastoquinone pool of chloroplast thylakoid membranes.-Physiol. Plantarum 140: 103-110, 2010. Go to original source...
    53. Nakano Y., Asada K.: Spinach chloroplasts scavenge hydrogen peroxide on illumination.-Plant Cell Physiol. 21: 1295-1307, 1980. Go to original source...
    54. Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control.-Annu. Rev. Plant Biol. 49: 249-279, 1998. Go to original source...
    55. Ogbaga C.C., Stepien P., Johnson G.N.: Sorghum (Sorghum bicolor) varieties adopt strongly contrasting strategies in response to drought.-Physiol. Plantarum 152: 389-401, 2014. Go to original source...
    56. Oliveira A.B., Gomes-Filho E.: Germination and vigor of sorghum seeds under water and salt stress.-Rev. Brasil. Sementes 31: 48-56, 2009. Go to original source...
    57. Osório M.L., Osório J., Romano A.: Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought.-Photosynthetica 51: 75-84, 2013.
    58. Ozkur O., Ozdemir F., Bor M. et al.: Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought.-Environ. Exp. Bot. 66: 487-492, 2009. Go to original source...
    59. Peever T.L., Higgins V.J.: Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum.-Plant Physiol. 90: 867-875, 1989. Go to original source...
    60. Plaut Z., Federman E.: Simple procedure to overcome polyethy lene glycol toxicity on whole plants.-Plant Physiol. 79: 559-561, 1985. Go to original source...
    61. Qin L.Q., Li L., Bi C. et al.: Damaging mechanisms of chillingand salt stress to Arachis hypogaea L. leaves.-Photosynthetica 49: 37-42, 2011. Go to original source...
    62. Reddy A.R., Chaitanya K.V., Vivekanandan M.: Droughtinduced responses of photosynthesis and antioxidant metabolism in higher plants.-J. Plant Physiol. 161: 1189-1202, 2004. Go to original source...
    63. Ren C.G., Li X., Liu X.L. et al.: 1-butanol regulating the stomatal movementthrough endogenous H2O2 in C4 pepc transgenic rice (Oryza sativa L.).-Plant Physiol. Bioch. 74: 218-229, 2014. Go to original source...
    64. Rooney W.L., Blumenthal J., Bean B. et al.: Designing sorghum as a dedicated bioenergy feedstock.-Biofuel. Bioprod. Bioref. 1: 147-157, 2007. Go to original source...
    65. Sairam R., Srivastava G.: Changes in antioxidant activity in subcellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress.-Plant Sci. 162: 897-904, 2002. Go to original source...
    66. Scandalios J.G.: Oxygen stress and superoxide dismutases.-Plant Physiol. 101: 7, 1993. Go to original source...
    67. Schansker G., Srivastava A., Govindjee, Strasser R.J.: Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves.-Funct. Plant Biol. 30: 785-796, 2003.
    68. Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis.-In: Schulze E.D., Caldwell M.M. (ed.): Ecophysiology of Photosynthesis, Vol. 100. Pp. 49-70, Springer, Dordrecht 1994. Go to original source...
    69. Slama I., Ghnaya T., Hessini K. et al.: Comparative study of the effects of mannitol and PEG osmotic stress on growth and solute accumulation in Sesuvium portulacastrum.-Environ. Exp. Bot. 61: 10-17, 2007. Go to original source...
    70. 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...
    71. Song X.S., Hu W.H., Mao W.H. et al.: Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L.-Plant Physiol. Bioch. 43: 1082-1088, 2005. Go to original source...
    72. Sui N.: Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water-water cycle.-Photosynthetica 53: 207-212, 2015. Go to original source...
    73. Taylor A., Motes J., Kirkham M.: Germination and seedling growth characteristics of three tomato species affected by water deficits [Lycopersicon chilense, Lycopersicon esculentum, Solanum pennellii].-J. Am. Soc. Hortic. Sci. 107: 282-285, 1982.
    74. Terzi R., Kadioglu A.: Drought stress tolerance and the antioxidant enzyme system.-Acta Biol. Cracov. Bot. 48: 89-96, 2006.
    75. van Kooten O., Snel J.F.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147-150, 1990. Go to original source...
    76. Wang A.G., Luo G.H.: Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants.-Plant Physiol. Commun. 6: 55-57, 1990.
    77. Xu C.C., Jeon Y.A., Lee C.H.: Relative contributions of photochemical and non photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature.-Physiol. Plantarum 107: 447-453, 1999. Go to original source...
    78. Yu J., Tuinstra M., Claassen M. et al.: Analysis of cold tolerance in sorghum under controlled environment conditions.-Field Crop. Res. 85: 21-30, 2004. Go to original source...
    79. Zavariyan A.M., Rad M.Y., Asghari M.: Effect of seed priming by pyridoxine on germination and biochemical indices in Silybum marianum L. under drought stress.-Int. J. Life Sci. 9: 17-22, 2015

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