Brassinosteroid alleviates chilling-induced oxidative stress in pepper by enhancing antioxidation systems and maintenance of photosystem II

• Autorzy: Li J. , Yang P. , Gan Y. , Yu J. , Xie J.
• Języki publikacji: EN

Abstrakty

EN

To explore regulated mechanisms of Brassinosteroids-induced chilling tolerance, we studied the involvement of foliar sprayed 24-epibrassinolide (EBR) in the growth, lipid peroxidation, distribution of absorbed energy and excitation energy, chlorophyll fluorescence characteristics and antioxidant defense system of pepper seedlings under chilling stress. We found that low temperature retarded the growth of pepper seedlings, but foliar spray of EBR solution markedly improved the photoinhibition by increasing maximum quantum efficiency of photosystem II (Fv/Fm), the actual photochemical efficiency of photosystem II, photochemical quenching coefficient and the efficiency of excitation capture of open PSII center (Fv'/Fm'). Likewise, EBR increased the fraction of photochemical efficiency (P) and reduced the fraction of antenna heat dissipation (D) and excess energy (E). Low temperature led the increase in end product of lipid peroxidation and the content of H2O2, O2 - and OH-, and it caused the occurrence of oxidative stress. The activities of antioxidative enzymes including superoxide dismutase, peroxidase, catalase and ascorbate peroxidase, and contents of ascorbic acid and reduced glutathione were significantly improved by EBR during low temperature stress. The application of EBR also markedly increased the contents of proline, soluble sugar and protein under low temperature. EBR significantly reinforced antioxidant defense system, and it can be reflected through the reduced accumulation of harmful reactive oxygen species and MDA in pepper seedlings. Overall, these results suggest that EBR increases the tolerance of pepper seedlings against chilling stress largely by optimizing distribution of absorbed energy and excitation energy and enhancing antioxidant defense system.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 11
• Opis fizyczny: Article: 222 [11 p.], fig.,ref.

Twórcy

autor

Li J.

• College of Horticulture, Gansu Agricultural University, Lanzhou, 730070, China

autor

Yang P.

• College of Agronomy, Gansu Agricultural University, Lanzhou, 730070, China

autor

Gan Y.

• Agriculture and Agri-Food Canada, Semiarid Prairie Agricultural Research Centre, Swift Current, SK, Canada

autor

Yu J.

• College of Horticulture, Gansu Agricultural University, Lanzhou, 730070, China

autor

Xie J.

• College of Horticulture, Gansu Agricultural University, Lanzhou, 730070, China

Bibliografia

• Ahammed GJ, Yuan HL, Ogweno JO, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ (2012) Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato. Chemosphere 86:546–555
• Ahammed GJ, Ruan YP, Zhou J, Xia XJ, Shi K, Zhou YH (2013) Brassinosteroid alleviates polychlorinated biphenyls-induced oxidative stress by enhancing antioxidant enzymes activity in tomato. Chemosphere 90:2645–2653
• Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054
• Allen DJ, Ort DR (2001) Impact of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42
• Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:382–388
• Andre CM, Yvan L, Daniele E (2010) Dietary antioxidants and oxidative stress from a human and plant perspective: a review. Curr Nutr Food Sci 6:2–12
• Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8
• Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
• Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
• Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543
• Bradford MM (1976) 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
• Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629
• Cao S, Xu Q, Cao Y, Qian K, An K, Zhu Y, Binzeng H, Zhao H, Kuai B (2005) Loss of function mutations in DET2 gene lead to an enhanced resistance to oxidative stress in Arabidopsis. Physiol Plant 123:57–66
• Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775
• Cui JX, Zhou YH, Ding JG, Xia XJ, Shi K, Chen SC, Asami T, Chen Z, Yu JQ (2011) Role of nitric oxide in hydrogen peroxidedependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell Environ 34:347–358
• Demmig-Adams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264
• Duan M, Feng HL, Wang LY, Li D, Meng QW (2012) Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol 169:867–877
• El-Bassiony AM, Ghoname AAA, El-Awadi ME, Fawzy ZF, Gruda N (2012) Ameliorative effects of brassinosteroids on growth and productivity of snap beans grown under high temperature. Gesunde Pflanzen 64:175–182
• Elsheery NI, Cao KF (2008) Gas exchange, chlorophyll fluorescence, and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol Plant 30:769–777
• Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620
• Fariduddin Q, Yusuf M, Chalkoo S, Hayat S, Ahmad A (2011) 28-homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica 49:55–64
• García-Plazaola JI, Hernández A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Funct Plant Biol 30:319–324
• Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31:292–308
• Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
• Giannopolitis CN, Ries SK (1977) Superoxide dismutase in higher plants. Plant Physiol 59:309–314
• Gray GR, Savitch LV, Ivanov AG, Huner N (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. (II. Adjustment of photosynthetic capacity in winter wheat and winter rye). Plant Physiol 110:61–71
• Griffith OW (1980) Determination of glutathione and glutathione disulphide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212
• Havaux M, Kloppstech K (2001) The protective functions of carotenoids and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213:953–966
• Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environ Exp Bot 69(2):105–112
• Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
• Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581–588
• Hu WH, Wu Y, Zeng JZ, He L, Zeng QM (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48:537–544
• Hussain MI, Reigosa MJ (2011) Allelochemical stress inhibits growth, leaf water relations, PSII photochemistry, nonphotochemical fluorescence quenching, and heat energy dissipation in three C3 perennial species. J Exp Bot 62:4533–4545
• Ivanov AG, Hurry V, Sane PV, Öquist G, Huner NPA (2008) Reaction centre quenching of excess light energy and photoprotection of photosystem II. J Plant Biol 51:85–96
• Jiang YP, Cheng F, Zhou YH, Xia XJ, Shi K, Yu JQ (2012) Interactive effects of CO2 enrichment and brassinosteroid on CO2 assimilation and photosynthetic electron transport in Cucumis sativus. Environ Exp Bot 75:98–106
• Kong FY, Deng YS, Zhou B, Wang G, Wang Y, Meng QW (2013) A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress. J Exp Bot 65:143–158
• Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. Photosynth Res 5:139–157
• Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297
• Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117
• Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903
• Li L, van Staden J, Jager AK (1998) Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. Plant Growth Regul 25:81–87
• Li J, Yang P, Xie JM, Yu JH (2015) Effects of 24-epibrassinolide on growth and antioxidant enzymes system in pepper roots under chilling stress. J Nuclear Agric Sci 29:1048–1055
• Liu YJ, Zhao ZG, Si J, Di CX, Han J, An LZ (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 59:207–214
• Liu YJ, Jiang HF, Zhao ZG, An LZ (2011) Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana. J Plant Physiol 168:853–862
• Liu ZX, Bie ZL, Huang Y, Zhen A, Lei B, Zhang HY (2012) Grafting onto Cucurbita moschata rootstock alleviates salt stress in cucumber plants by delaying photoinhibition. Photosynthetica 50:152–160
• Ma NN, Zuo YQ, Liang XQ, Yin B, Wang GD, Meng QW (2013) The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. Physiol Plant 149:474–486
• Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668
• Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
• Núñez M, Mazzafera P, Mazzora LM, Sigueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70
• Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogués S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57
• Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882
• Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288
• Schwitzguébel JP, Page V, Martins-Dias S, Davies LC, Vasilyeva G, Strijakova E (2011) Using plants to remove foreign compounds from contaminated water and soil. In: Schroder P, Collins CD (eds) Organic xenobiotics and plants, plant ecophysiology, vol 8. Springer, Netherlands, pp 149–189
• Shahbaz M, Ashraf M, Athar HR (2008) Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? Plant Growth Regul 55:51–64
• Sharma I, Pati PK, Bhardwaj R (2011) Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 33:1723–1735
• van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
• Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24:842–857
• Wang BK, Zeng GW (1993) Effect of epibrassinolide on the resistance of rice seedlings to chilling injury. J Plant Physiol Mol Biol 19:38–42
• Wang QR, Klassen W, Evans EA, Li YC, Codallo M (2010) Combination of organic and plastic mulches to improve the yield and quality of winter fresh market bell peppers (Capsicum annuum L.). HortScience 45:701–706
• Weng JH, Jhaung LH, Jiang JY, Lai GM, Liao TS (2006) Downregulation of photosystem 2 efficiency and spectral reflectance in mango leaves under very low irradiance and varied chilling treatments. Photosynthetica 44:248–254
• Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816
• Wu XX, Yao XF, Chen JL, Zhu ZW, Zhang H, Zha DS (2014) Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiologiae Plant 36:251–261
• Xi ZM, Wang ZZ, Fang YL, Hu ZY, Hu Y, Deng MM, Zhang ZW (2013) Effects of 24-epibrassinolide on antioxidation defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regul 71:57–65
• Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen ZX, Yu JQ (2009a) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196
• Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009b) Reactive oxygen species are involved in Brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814
• Yuan GF, Jia CG, Li Z, Sun B, Zhang LP, Liu N, Wang QM (2010) Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci Hortic 126:103–108
• Yusuf M, Fariduddin Q, Ahmad A (2012) 24-epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiata under different levels of nickel: a shotgun approach. Plant Physiol Biochem 57:143–153
• Zhang MC, Zhai ZX, Tian XL, Duan LS, Li ZH (2008) Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regul 56:257–264

Identyfikatory

DOI

10.1007/s11738-015-1966-9