Scientia Agricultura Sinica ›› 2014, Vol. 47 ›› Issue (6): 1171-1179.doi: 10.3864/j.issn.0578-1752.2014.06.013

• HORTICULTURE • Previous Articles     Next Articles

Heat Stress Mitigation by Exogenous Nitric Oxide Application Involves Polyamine Metabolism and PSII Physiological Strategies in Ginger Leaves

 LI  Xiu, GONG  Biao, WANG  Yun, XU  Kun   

  1. College of Horticulture Science and Engineering, Shandong Agricultural University/State Key Laboratory of Crop Biology/Key Laboratory of Biology and Genetic Improvement of Horticultural Crops in Huanghuai Region, Taian 271018, Shandong
  • Received:2013-09-29 Online:2014-03-15 Published:2013-12-25

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Abstract: 【Objective】 Ginger is a thermophilic vegetable crop with the characteristics of not tolerating high temperature, which is easily damaged by high temperature. To investigate the relationship between exogenous nitric oxide and polyamine metabolism, as well as the regulation effect on PSII, mitigation effect of heat stress on ginger by nitric oxide was studied. 【Method】‘Laiwu Big Ginger’ was sandy cultured in a climate chamber under 12h/12h photoperiod, 28℃/18℃ (normal) and 38℃/28℃ (heat stress) conditions. Ginger root was treated with 0.1 mmol•L-1 sodium nitroprussiate (an nitric oxide donor) and sodium ferricyanide (reactant of SNP after releasing NO). Relative water content, chlorophyll concentration, electrolyte leakage, chlorophyll fluorescence parameters and polyamine metabolism of ginger leaves were investigated on 0, 5, 10, 15 and 20 d after treatment. 【Result】Electrolyte leakage significantly increased with prolonging stressed time, while relative water content and chlorophyll concentration significantly decreased. Chlorophyll fluorescence parameters including Fv/Fm, ФPSII, Fv′/Fm′ qP and P decreased, and NPQ, β/α-1 and D increased. Main pattern of PSII was shown that its photochemical activity of PSII was decreased for the energy metabolism pathway shifting from photochemical to non-photochemical activity. Under heat stress, free and conjugated polyamines were significantly accumulated and then decreased in different treatment times. Insoluble bound polyamine and Put/PAs ratio kept an increasing trend with prolonging stressed time. Relative water content, chlorophyll concentration, electrolyte leakage of ginger leaves was recovered by exogenous application of nitric oxide, which regulated chlorophyll fluorescence parameters to normalization. Also nitric oxide application improved polyamine metabolism to reduce Put/PAs ratio. 【Conclusion】 Disordered polyamine metabolism, damaged ginger leaves and PSII were shown under 38℃/28℃ conditions. Significant heat stress mitigation by exogenous nitric oxide application was shown in this research involving polyamine metabolism and PSII physiological strategies to improve heat stress tolerance in ginger.

Key words: ginger , heat stress , nitric oxide , psII , polyamine metabolism

[1]赵德婉, 徐坤, 艾希珍, 郭衍银, 郑永强. 生姜高产栽培技术. 2版. 北京: 金盾出版社, 2005.

Zhao D W, Xu K, Ai X Z, Guo Y Y, Zheng Y Q. High-yield Cultivation Techniques of Ginger. 2nd edition. Beijing: Jindun Press, 2005. (in Chinese)

[2]彭燕，黄炳茹，许立新，李州. 高温胁迫对草地早熟禾渗透势、膜脂肪酸成分及膜脂过氧化产物的影响. 园艺学报, 2013, 40 (5): 971-980.

Peng Y, Huang B R, Xu L X, Li Z. Heat stress effects on osmotic potential, membrane fatty acid composition and lipid peroxidation content of two Kentucky bluegrass cultivars differing in drought tolerance. Acta Horticulturae Sinica, 2013, 40 (5): 971-980. (in Chinese)

[3]Berry J A, Björkman O. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology, 1980, 31: 491-543.

[4]Genty B, Briantais J M, Baker N R. The relationship between the quantum yield of photosynthesis electron transport and quenching of chlorophyll fluorescence. Biochemica et Biophysica Acta, 1989, 990(1): 87-92.

[5]Pospíil P, Tyystjärvi E. Molecular mechanism of high temperature- induced inhibition of acceptor side of photosystem II. Photosynthesis Research, 1999, 62(1): 55-66.

[6]Kouil R, Lazár D, Ilík P, Skotnica J, Krch ák P, Nau J. High temperature-induced chlorophyll fluorescence rise in plants at 40–50℃: experimental and theoretical approach. Photosynthesis Research, 2004, 81(1): 49-66.

[7]汪炳良, 徐敏, 史庆华, 曹家树. 高温胁迫对早熟花椰菜叶片抗氧化系统和叶绿素及其荧光参数的影响. 中国农业科学, 2004, 37(8): 1245-1250.

Wang B L, Xu M, Shi Q H, Cao J S. Effects of high temperature stress on antioxidant systems, chlorophyll and chlorophyll flrorescence parameters in early cauliflower leaves. Scientia Agricultura Sinica, 2004, 37(8): 1245-1250. (in Chinese)

[8]Arasimowicz M, Floryszak-Wieczorek J. Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Science, 2007, 172(5): 876-887.

[9]Xuan Y, Zhou S, Wang L, Cheng Y D, Zhao L Q. Nitric oxide functions as a signal and acts upstream of AtCAM3 in thermotolerance in Arabidopsis seedlings. Plant Physiology, 2010, 153(4): 1895-1906.

[10]Uchida A, Jagendorf A T, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science, 2002, 163(3): 515-523.

[11]Song L, Ding W, Zhao M, Sun B, Zhang L. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Science, 2006, 171(4): 449-458.

[12]García-Mata C, Lamattina L. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology, 2001, 126(3): 1196-1204.

[13]Liu F, Guo F Q. Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark- induced leaf senescence in Arabidopsis. PLOS One, 2013, 8(2): 1-12.

[14]Hossain K K, Nakamura T, Yamasaki H. Effect of nitric oxide on leaf non-photochemical quenching of fluorescence under heat-stress conditions. Russian Journal of Plant Physiology, 2011, 58(4): 629-633.

[15]Duca S, Tidu V, Bassi R, Esposito C, Serafini-Fracassini D. Identification of chlorophyll-a/b proteins as substrates of transglutaminase activity in isolated chloroplasts of Helianthus tuberosus L. Planta, 1994, 193: 283-289.

[16]He L X, Nada K, Yoshihisa K, Tachibana S. Enhanced susceptibility of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of Spinach (Spinacia oleracea L.). Plant Cell Physiology, 2002, 43(2): 196-206.

[17]Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubis J. Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber. Journal of Plant Growth Regualtion, 2009, 28(2): 177-186.

[18]Filippou P, Antoniou C, Fotopulos V. The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radical Biology and Medicine, 2013, 56: 172-183.

[19]Yamasaki T, Yamakawa T, Yamane Y, Koike H, Satoh K, Katoh S. Temperature acclimation of photosynthesis and related changes in photosystem II electron transport in winter wheat. Plant Physiology, 2002, 128(3): 1087-1097.

[20]Barrs H D, Weatherley P E. Are-examination of the relative turgidity techniques for estimating water deficits in leaves. Australian Journal of Biological Sciences, 1962, 15(3): 413-428.

[21]曹刚, 张国斌, 郁继华, 马彦霞. 不同光质LED光源对黄瓜苗期生长及叶绿素荧光参数的影响. 中国农业科学, 2013, 46(6): 1297-1304.

Cao G, Zhang G B, Yu J H, Ma Y X. Effects of different LED light qualities on cucumber seedling growth and chlorophyll fluorescence parameters. Scientia Agricultura Sinica, 2013, 46(6): 1297-1304. (in Chinese)

[22]Braun G, Malkin S. Regulation of the imbalance in light excitation between photosystem II and photosystem I by cations and by the energized state of the thylakoid membrance. Biochimica et Biophysica Acta. 1990, 1017(1): 79-90.

[23]Demmig-Adams B, Adams III W W, Baker D H, Logan B A, Bowling D R, Verhoeven A S. Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum, 1996, 98(2): 253-264.

[24]Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J. Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress. Plant Physiology and Biochemistry, 2012, 57: 200-209.

[25]Ederli L, Reale L, Madeo L, Ferranti F, Gehring C, Fornaciari M, Romano B, Pasqualini S. NO release by nitric oxide donors in vitro and in planta. Plant Physiology and Biochemistry, 2009, 47(1): 42-48.

[26]孙宪芝, 郭先锋, 郑成淑, 王文莉, 梁芳. 高温胁迫下外源钙对菊花叶片光合机构与活性氧清除酶系统的影响. 应用生态学报, 2008, 19(9): 1983-1988.

Sun X Z, Guo X F, Zheng C S, Wang W L, Liang F. Effects of exogenous Ca2+ on leaf photosynthetic apparatus and active oxygen scavenging enzyme system of chrysanthemum under high temperature stress. Chinese Journal of Applied Ecology, 2008, 19(9): 1983-1988. (in Chinese)

[27]张桂莲, 陈立云, 张顺堂, 刘国华, 唐文邦, 贺治洲, 王明. 抽穗开花期高温对水稻剑叶理化特性的影响. 中国农业科学, 2007, 40(7): 1345-1352.

Zhang G L, Chen L Y, Zhang S T, Liu G H, Tang W B, He Z Z, Wang M. Effects of high temperature on physiological and biochemical characteristics in flag leaf of rice during heading and flowering period. Scientia Agricultura Sinica, 2007, 40(7): 1345-1352. (in Chinese)

[28]Liu K, Fu H, Bei Q, Luan S. Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiology, 2000, 124(3): 1315-1325.

[29]Beligni M V, Fath A, Bethbe P C, Lamattina L, Jones R L. Nitric oxide acts as an antioxidant and delays programmed cell death in barely aleurone layers. Plant Physiology, 2002, 129(4): 1642-1650.

[30]He J X, Wang J, Liang H G. Effects of water on photochemical function and protein metabolism of photosystem II in wheat leaves. Plant Physiology, 1995, 93(4): 771-777.

[31]Barnabas B, Gager K, Feher A. The effect of drought and heat stress on reproductive processes in cereals. Plant and Cell Environment, 2008, 31(1): 11-38.

[32]Shu S, Yuan L Y, Guo S R, Sun J, Yuan Y H. Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiology and Biochemistry, 2013, 63: 209-216.

[33]苏秀荣, 王秀峰, 杨凤娟, 魏珉. 硝酸根胁迫对黄瓜幼苗叶片光合速率、PSII光化学效率及光能分配的影响. 应用生态学报, 2007, 18(7): 1441-1446.

Su X R, Wang X F, Yang F J, Wei M. Effects of NO3- stress on photosynthetic rate, photochemical efficiency of PSII and light energy allocation in cucumber seedling leaves. Chinese Journal of Applied Ecology, 2007, 18(7): 1441-1446. (in Chinese)

[34]魏海荣, 孟艳玲, 孙阳, 刘庆忠. 高温胁迫下外源NO对高灌蓝莓PSII光化学活性和抗氧化系统的影响. 应用生态学报, 2010, 21(10): 2529-2535.

Wei H R, Meng Y L, Sun Y, Liu Q Z. Effects of exogenous nitric oxide on high bush blueberry PSII photochemical activity and antioxidant system under high temperature stress. Chinese Journal of Applied Ecology, 2010, 21(10): 2529-2535. (in Chinese)

[35]Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A F. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta, 2010, 231(6): 1237-1249.

[36]Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L. Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. The Plant Cell, 2010, 22(11): 3816-3830.

[37]段九菊, 郭世荣, 康云艳, 李璟, 刘香娥. 盐胁迫对黄瓜幼苗根系生长和多胺代谢的影响. 应用生态学报, 2008, 19(1): 57-64.

Duan J J，Guo S R, Kang Y Y, Li J, Liu X E. Effect of salt stress on cucumber seedlings root growth and polyamine metabolism. Chinese Journal of Applied Ecology, 2008, 19(1): 57-64. (in Chinese)

[38]Sagor G H M, Berberich T, Takahashi Y, Niitsu M, Kusano T. The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Research, 2013, 22(3): 595-605.

[39]Brüggemann L I, Pottosin I I, Schonknecht G. Cytoplasmic polyamines block the fast-activating vacuolar cation channel. The Plant Journal, 1998, 16(1): 101-105.

[40]Gill S S, Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signaling and Behavior, 2010, 5(1): 26-33.
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