干旱和低温胁迫下细胞外ATP对当归幼苗叶绿素含量及其荧光特性的调节
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摘要
细胞外ATP(eATP)作为一种重要的信号分子,能调节植物逆境胁迫下的多种生理生化反应。该研究以当归幼苗作为实验材料,分析了干旱胁迫和低温胁迫下细胞外ATP(eATP)对叶绿素含量及叶绿素荧光参数变化特性的调节作用。研究发现,干旱和低温胁迫都能引起当归叶片的叶绿素含量、实际光化学效率[Y(Ⅱ)]、光系统Ⅱ(PSⅡ)电子传递速率(ETR)、光化学淬灭系数(qP,qL)显著降低,同时也引起非光化学猝灭(qN,NPQ)显著增加。外源ATP的应用减轻了干旱和低温胁迫下当归叶片叶绿素含量,Y(Ⅱ),ETR,qP,qL,eATP水平的降低,同时也消除了qN和NPQ的增加。以上结果表明,在干旱和低温胁迫下eATP可有效增加PSⅡ反应中心的开放比例,提高当归叶片光系统Ⅱ的电子传递速率和光能转化效率,有利于增强当归幼苗叶绿素合成以及光系统Ⅱ对干旱和低温胁迫的适应性。
As an important signal molecule, extracellular ATP(eATP) can regulate many physiological and biochemical responses to plant stress. In this study, the regulation of extracellular ATP(eATP) on chlorophyll content and chlorophyll fluorescence parameters of Angelica sinensis seedlings were studied under drought and low temperature stress. The results showed that all the chlorophyll content, the actual photochemical efficiency [Y(Ⅱ)], the electron transfer rate(ETR), the photochemical quenching coefficient(qP and qL) of A. sinensis leaves were significantly decreased under drought and low temperature stress, respectively. At the same time, non-photochemical quenching(NPQ and qN) were also all significantly increased, respectively. The application of eATP alleviated the decrease of chlorophyll content, Y(Ⅱ), ETR, qP and qL of A. sinensis leaves under drought and low temperature stress, and eliminated the increase of qN and NPQ. The results indicated that eATP could effectively increase the open ratio of PSⅡ reaction centers, and improve the electron transfer rate and light energy conversion efficiency of PSⅡ of A. sinensis leaves under drought and low temperature stress. It is beneficial to enhance the chlorophyll synthesis and the adaptability of PSⅡ about A. sinensis seedlings to drought and low temperature stress.
As an important signal molecule, extracellular ATP(eATP) can regulate many physiological and biochemical responses to plant stress. In this study, the regulation of extracellular ATP(eATP) on chlorophyll content and chlorophyll fluorescence parameters of Angelica sinensis seedlings were studied under drought and low temperature stress. The results showed that all the chlorophyll content, the actual photochemical efficiency [Y(Ⅱ)], the electron transfer rate(ETR), the photochemical quenching coefficient(qP and qL) of A. sinensis leaves were significantly decreased under drought and low temperature stress, respectively. At the same time, non-photochemical quenching(NPQ and qN) were also all significantly increased, respectively. The application of eATP alleviated the decrease of chlorophyll content, Y(Ⅱ), ETR, qP and qL of A. sinensis leaves under drought and low temperature stress, and eliminated the increase of qN and NPQ. The results indicated that eATP could effectively increase the open ratio of PSⅡ reaction centers, and improve the electron transfer rate and light energy conversion efficiency of PSⅡ of A. sinensis leaves under drought and low temperature stress. It is beneficial to enhance the chlorophyll synthesis and the adaptability of PSⅡ about A. sinensis seedlings to drought and low temperature stress.
引文
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[2] Fang L, Xiao X F, Liu C X, et al. Recent advance in studies on Angelica sinensis [J]. Chin Herbal Med, 2012, 4 (1): 12.
[3] 刘学周, 康天兰. 当归栽培新技术研究综述[J]. 甘肃农业科技, 2016(11):62.
[4] 张强. 中国西北干旱气候变化对农业与生态影响及对策 [M]. 北京:气象出版社, 2012.
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[6] Bradford K J, Hsiao T C. Physiological responses to moderate water stress[J]. Physiol Plant Ecol, 1982, 12:263.
[7] Graan T, Boyer J S. Very high CO2 partially restores photosynthesis in sunflower at low water potentials[J]. Planta, 1990, 181(3):378.
[8] Lauer M J, Boyer J S. Internal CO2 measured directly in leaves: abscisic acid and low leaf water potential cause opposing effects[J]. Plant Physiol, 1992, 98(4):1310.
[9] Lu C, Zhang J. Effects of water stress on photosystem Ⅱ photochemistry and its thermostability in wheat plants[J]. J Exp Bot, 1999, 50(336):1199.
[10] Havaux M, Canaani O, Malkin S. Photosynthetic responses of leaves to water stress, expressed by photoacoustics and related methods: Ⅱ. The effect of rapid drought on the electron transport and the relative activities of the two photosystems[J]. Plant Physiol, 1986, 82(3):827.
[11] Toivonen P, Vidaver W. Variable chlorophyll a fluorescence and CO(2) uptake in water-stressed white spruce seedlings[J]. Plant Physiol, 1988, 86(3):744.
[12] Havaux M, Canaani O, Malkin S. Inhibition of photosynthetic activities under slow water stress measured in vivo by the photoacoustic method[J]. Physiol Plantarum, 1987, 70(3):503.
[13] He J X, Wang J, Liang H G. Effects of water stress on photochemical function and protein metabolism of photosystem Ⅱ in wheat leaves[J]. Physiol Plantarum, 1995, 93(4):771.
[14] Thomas D S, Turner D W. Banana (Musa sp.) leaf gas exchange and chlorophyll fluorescence in response to soil drought, shading and lamina folding[J]. Sci Horticult, 2001, 90(1):93.
[15] Aranda I, Castro L, Pardos M, et al. Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak (Quercus suber, L.) seedlings[J]. Forest Ecol Manag, 2005, 210(1):117.
[16] Zivcak M, Kalaji H M, Shao H B, et al. Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress[J]. J Photochem Photobiol B, 2014, 137(SI):107.
[17] Maxwell K, Johnson G N. Chlorophyll fluorescence--a practical guide[J]. J Exp Bot, 2000, 51(345):659.
[18] Kopsell D A, Lefsrud M G, Kopsell D E, et al. Air temperature affects biomass and carotenoid pigment accumulation in kale and spinach grown in a controlled environment[J]. Hortsci Public American Soc Horticult Sci, 2005, 40(7):2026.
[19] Hikosaka K, Ishikawa K, Borjigidai A, et al. Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate[J]. J Exp Bot, 2006, 57(2):291.
[20] 赵停,李静,彭亮,等.钠盐胁迫对远志种子萌发特性的影响[J].中国实验方剂学杂志,2018,24(17):60.
[21] Roux S J, Steinebrunner I. Extracellular ATP: an unexpected role as a signaler in plants[J]. Trends Plant Sci, 2007, 12(11): 522.
[22] Kiwamu T, Simon G, Gary S, et al. Extracellular ATP signaling in plants[J]. Trends Cell Biol, 2010, 20(10):601.
[23] Wolf C, Hennig M, Romanovicz D, et al. Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants[J]. Plant Mol Biol, 2007, 64(6):657.
[24] Chivasa S, Murphy A M, Hamilton J M, et al. Extracellular ATP is a regulator of pathogen defence in plants[J]. Plant J, 2009, 60(3):436.
[25] Jeter C R, Tang W, Henaff E, et al. Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis[J]. Plant Cell, 2004, 16(10):2652.
[26] Song C J, Steinebrunner I, Wang X, et al. Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis[J]. Plant Physiol, 2006, 140(4):1222.
[27] Wu S J, Liu Y S, Wu J Y. The signaling role of extracellular ATP and its dependence on Ca2+ flux in elicitation of Salvia miltiorrhiza hairy root cultures[J]. Plant Cell Physiol, 2008, 49(4):617.
[28] Steinebrunner I, Wu J, Sun Y, et al. Disruption of apyrases inhibits pollen germination in Arabidopsis[J]. Plant Physiol, 2003, 131(4): 1638.
[29] Wu J, Steinebrunner I, Sun Y, et al. Apyrases(nucleoside triphosphate diphosphohydrolases) play a keyrole in growth control in Arabidopsis[J]. Plant Physiol, 2007, 144(2): 961.
[30] Riewe D, Grosman L, Fernie A R, et al. The potato-specific apyrase is apoplastically localized and hasinfluence on gene expression, growth, and development[J]. Plant Physiol, 2008, 147(3): 1092.
[31] Clark G, Torres J, Finlayson S, et al. Apyrase (nucleoside triphosphate diphosphohydrolase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules[J]. Plant Physiol, 2010,152(2):1073.
[32] Sun J, Zhang C L, Deng S R, et al. An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica[J]. Plant Cell Environ, 2012, 35(5): 893.
[33] Foresi N P, Laxalt A M, Tonon C V, et al. Extracellular ATP induces nitric oxide production in tomatocell suspensions[J]. Plant Physiol, 2007, 145(3): 589.
[34] Chivasa S, Ndimba B K, Simon W J, et al. Extracellular ATP functions as an endogenous externalmetabolite regulating plant cell viability[J]. Plant Cell, 2006,17(11): 3019.
[35] Tanaka K, Choi J, Cao Y, et al. Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants[J]. Front Plant Sci, 2014, 5:446.
[36] Demidchik V, Shang Z, Shin R. Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels[J]. Plant J, 2009,58(6): 903.
[37] Demidchik V, Cuin T A, Svistunenko D, et al. Arabidopsis root K+-efflux conductance activated byhydroxyl radicals: single channel properties, genetic basis and involvement in stress induced cell death[J].J Cell Sci, 2010, 123(9): 1468.
[38] Chivasa S, Simon W J, Murphy A M, et al. The effects of extracellular adenosine 5′-triphosphate on thetobacco proteome[J]. Proteomics, 2010, 10(2): 235.
[39] Feng H Q, Jiao Q S, Sun K, et al. Extracellular ATP affects chlorophyll fluorescence of kidney bean (Phaseolus vulgaris) leaves through Ca 2+, and H2 O2 -dependent mechanism[J]. Photosynthetica, 2015, 53(2):201.
[40] Arnon D I. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris[J]. Plant Physiol,1949, 24(l):1.
[41] Flexas J, Escalona J M, Medrano H. Water stress induces different levels of photosynthesis and electron transport rate regulation ingrapevines[J].Plant Cell Environ, 1999, 22(1):39.
[42] Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy S A, et al. Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L[J]. Plant Physiol Bioch, 2016, 106:141.
[43] Mittler R. Abiotic stress, the field environment and stress combination[J]. Trends Plant Sci, 2006, 11(1):15.
[44] Ibáňez H, Ballester A,Muňoz R, et al.Chloroespiration and tolerance to drought, heat and high illumination[J].Plant Physiol,2010, 167(9):732.
[45] Jagtap V, Bhargava S, Streb P, et al. Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) Moench[J]. J Exp Bot, 1998, 49(327):1715.
[46] Naumann J C, Young D R, Anderson J E. Linking leaf chlorophyll fluorescence properties to physiological responses for detection of salt and drought stress in coastal plant species[J]. Physiol Plantarum, 2010, 131(3):422.
[47] 李文娆,张岁岐,山仑.水分胁迫对紫花苜蓿根系吸水与光合特性的影响[J].草地学报,2007, 15(3):207.
[48] 王利军, 马履一, 王爽,等. 水盐胁迫对沙枣幼苗叶绿素荧光参数和色素含量的影响[J]. 西北农业学报, 2010, 19(12):122.
[49] Baker N R, Rosenqvist E.Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities[J]. J Exp Bot, 2004, 55(403):1607.
[50] Calatayud A, Roca D, Martínez P F.Spatial-temporal variations in rose leaves under water stress conditions studied by chlorophyll fluorescence imaging[J]. Plant Physiol Biochem, 2006, 44(10):564.
[51] 杨扬, 王晓燕, 王江, 等. 物种多样性对植物生长与土壤镉污染修复的影响[J]. 环境科学学报,2016, 36(6): 2103.
[52] 冯鹏, 孙力, 申晓慧, 等. 多年生黑麦草对Pb、Cd胁迫的响应及富集能力研究[J]. 草业学报, 2016, 25(1): 153.
[53] Miyake C, Horiguchi S, Makino A, et al. Effects of light intensity on cyclic electron flow around psi and its relationship to non-photochemical quenching of chl fluorescence in tobacco leaves[J]. Plant Cell Physiol, 2005, 46(11):1819.
[54] 石岱龙, 田武英, 焦青松,等. 外源ATP对NaCl胁迫下菜豆叶片叶绿素荧光特性的调节[J]. 广西植物, 2016, 36(9):1087.
[55] Ashraf M, Harris P J C. Photosynthesis under stressful environments: an overview[J]. Photosynthetica, 2013, 51(2):163.
[56] Herrera A, Fernández M D, Taisma M A. Effects of drought on CAM and water relations in plants of Peperomia carnevalii[J]. Ann Bot, 2000, 86(3):511.
[57] Adams W W, Osmond C B, Sharkey T D.Responses of two CAM species to different irradiances during growth and susceptibility to photoinhibition by high light[J].Plant Physiol, 1987, 83(1):213.
[58] Kaiser W M. Effects of water deficit on photosynthetic capacity[J]. Physiol Plantarum, 1987, 71(1):142.
[2] Fang L, Xiao X F, Liu C X, et al. Recent advance in studies on Angelica sinensis [J]. Chin Herbal Med, 2012, 4 (1): 12.
[3] 刘学周, 康天兰. 当归栽培新技术研究综述[J]. 甘肃农业科技, 2016(11):62.
[4] 张强. 中国西北干旱气候变化对农业与生态影响及对策 [M]. 北京:气象出版社, 2012.
[5] 武延安, 蔺海明, 赵贵宾, 等. 遮光对当归栽培的效应 [J]. 中药材, 2008, 31 (3): 334.
[6] Bradford K J, Hsiao T C. Physiological responses to moderate water stress[J]. Physiol Plant Ecol, 1982, 12:263.
[7] Graan T, Boyer J S. Very high CO2 partially restores photosynthesis in sunflower at low water potentials[J]. Planta, 1990, 181(3):378.
[8] Lauer M J, Boyer J S. Internal CO2 measured directly in leaves: abscisic acid and low leaf water potential cause opposing effects[J]. Plant Physiol, 1992, 98(4):1310.
[9] Lu C, Zhang J. Effects of water stress on photosystem Ⅱ photochemistry and its thermostability in wheat plants[J]. J Exp Bot, 1999, 50(336):1199.
[10] Havaux M, Canaani O, Malkin S. Photosynthetic responses of leaves to water stress, expressed by photoacoustics and related methods: Ⅱ. The effect of rapid drought on the electron transport and the relative activities of the two photosystems[J]. Plant Physiol, 1986, 82(3):827.
[11] Toivonen P, Vidaver W. Variable chlorophyll a fluorescence and CO(2) uptake in water-stressed white spruce seedlings[J]. Plant Physiol, 1988, 86(3):744.
[12] Havaux M, Canaani O, Malkin S. Inhibition of photosynthetic activities under slow water stress measured in vivo by the photoacoustic method[J]. Physiol Plantarum, 1987, 70(3):503.
[13] He J X, Wang J, Liang H G. Effects of water stress on photochemical function and protein metabolism of photosystem Ⅱ in wheat leaves[J]. Physiol Plantarum, 1995, 93(4):771.
[14] Thomas D S, Turner D W. Banana (Musa sp.) leaf gas exchange and chlorophyll fluorescence in response to soil drought, shading and lamina folding[J]. Sci Horticult, 2001, 90(1):93.
[15] Aranda I, Castro L, Pardos M, et al. Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak (Quercus suber, L.) seedlings[J]. Forest Ecol Manag, 2005, 210(1):117.
[16] Zivcak M, Kalaji H M, Shao H B, et al. Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress[J]. J Photochem Photobiol B, 2014, 137(SI):107.
[17] Maxwell K, Johnson G N. Chlorophyll fluorescence--a practical guide[J]. J Exp Bot, 2000, 51(345):659.
[18] Kopsell D A, Lefsrud M G, Kopsell D E, et al. Air temperature affects biomass and carotenoid pigment accumulation in kale and spinach grown in a controlled environment[J]. Hortsci Public American Soc Horticult Sci, 2005, 40(7):2026.
[19] Hikosaka K, Ishikawa K, Borjigidai A, et al. Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate[J]. J Exp Bot, 2006, 57(2):291.
[20] 赵停,李静,彭亮,等.钠盐胁迫对远志种子萌发特性的影响[J].中国实验方剂学杂志,2018,24(17):60.
[21] Roux S J, Steinebrunner I. Extracellular ATP: an unexpected role as a signaler in plants[J]. Trends Plant Sci, 2007, 12(11): 522.
[22] Kiwamu T, Simon G, Gary S, et al. Extracellular ATP signaling in plants[J]. Trends Cell Biol, 2010, 20(10):601.
[23] Wolf C, Hennig M, Romanovicz D, et al. Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants[J]. Plant Mol Biol, 2007, 64(6):657.
[24] Chivasa S, Murphy A M, Hamilton J M, et al. Extracellular ATP is a regulator of pathogen defence in plants[J]. Plant J, 2009, 60(3):436.
[25] Jeter C R, Tang W, Henaff E, et al. Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis[J]. Plant Cell, 2004, 16(10):2652.
[26] Song C J, Steinebrunner I, Wang X, et al. Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis[J]. Plant Physiol, 2006, 140(4):1222.
[27] Wu S J, Liu Y S, Wu J Y. The signaling role of extracellular ATP and its dependence on Ca2+ flux in elicitation of Salvia miltiorrhiza hairy root cultures[J]. Plant Cell Physiol, 2008, 49(4):617.
[28] Steinebrunner I, Wu J, Sun Y, et al. Disruption of apyrases inhibits pollen germination in Arabidopsis[J]. Plant Physiol, 2003, 131(4): 1638.
[29] Wu J, Steinebrunner I, Sun Y, et al. Apyrases(nucleoside triphosphate diphosphohydrolases) play a keyrole in growth control in Arabidopsis[J]. Plant Physiol, 2007, 144(2): 961.
[30] Riewe D, Grosman L, Fernie A R, et al. The potato-specific apyrase is apoplastically localized and hasinfluence on gene expression, growth, and development[J]. Plant Physiol, 2008, 147(3): 1092.
[31] Clark G, Torres J, Finlayson S, et al. Apyrase (nucleoside triphosphate diphosphohydrolase) and extracellular nucleotides regulate cotton fiber elongation in cultured ovules[J]. Plant Physiol, 2010,152(2):1073.
[32] Sun J, Zhang C L, Deng S R, et al. An ATP signalling pathway in plant cells: extracellular ATP triggers programmed cell death in Populus euphratica[J]. Plant Cell Environ, 2012, 35(5): 893.
[33] Foresi N P, Laxalt A M, Tonon C V, et al. Extracellular ATP induces nitric oxide production in tomatocell suspensions[J]. Plant Physiol, 2007, 145(3): 589.
[34] Chivasa S, Ndimba B K, Simon W J, et al. Extracellular ATP functions as an endogenous externalmetabolite regulating plant cell viability[J]. Plant Cell, 2006,17(11): 3019.
[35] Tanaka K, Choi J, Cao Y, et al. Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants[J]. Front Plant Sci, 2014, 5:446.
[36] Demidchik V, Shang Z, Shin R. Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels[J]. Plant J, 2009,58(6): 903.
[37] Demidchik V, Cuin T A, Svistunenko D, et al. Arabidopsis root K+-efflux conductance activated byhydroxyl radicals: single channel properties, genetic basis and involvement in stress induced cell death[J].J Cell Sci, 2010, 123(9): 1468.
[38] Chivasa S, Simon W J, Murphy A M, et al. The effects of extracellular adenosine 5′-triphosphate on thetobacco proteome[J]. Proteomics, 2010, 10(2): 235.
[39] Feng H Q, Jiao Q S, Sun K, et al. Extracellular ATP affects chlorophyll fluorescence of kidney bean (Phaseolus vulgaris) leaves through Ca 2+, and H2 O2 -dependent mechanism[J]. Photosynthetica, 2015, 53(2):201.
[40] Arnon D I. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris[J]. Plant Physiol,1949, 24(l):1.
[41] Flexas J, Escalona J M, Medrano H. Water stress induces different levels of photosynthesis and electron transport rate regulation ingrapevines[J].Plant Cell Environ, 1999, 22(1):39.
[42] Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy S A, et al. Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L[J]. Plant Physiol Bioch, 2016, 106:141.
[43] Mittler R. Abiotic stress, the field environment and stress combination[J]. Trends Plant Sci, 2006, 11(1):15.
[44] Ibáňez H, Ballester A,Muňoz R, et al.Chloroespiration and tolerance to drought, heat and high illumination[J].Plant Physiol,2010, 167(9):732.
[45] Jagtap V, Bhargava S, Streb P, et al. Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) Moench[J]. J Exp Bot, 1998, 49(327):1715.
[46] Naumann J C, Young D R, Anderson J E. Linking leaf chlorophyll fluorescence properties to physiological responses for detection of salt and drought stress in coastal plant species[J]. Physiol Plantarum, 2010, 131(3):422.
[47] 李文娆,张岁岐,山仑.水分胁迫对紫花苜蓿根系吸水与光合特性的影响[J].草地学报,2007, 15(3):207.
[48] 王利军, 马履一, 王爽,等. 水盐胁迫对沙枣幼苗叶绿素荧光参数和色素含量的影响[J]. 西北农业学报, 2010, 19(12):122.
[49] Baker N R, Rosenqvist E.Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities[J]. J Exp Bot, 2004, 55(403):1607.
[50] Calatayud A, Roca D, Martínez P F.Spatial-temporal variations in rose leaves under water stress conditions studied by chlorophyll fluorescence imaging[J]. Plant Physiol Biochem, 2006, 44(10):564.
[51] 杨扬, 王晓燕, 王江, 等. 物种多样性对植物生长与土壤镉污染修复的影响[J]. 环境科学学报,2016, 36(6): 2103.
[52] 冯鹏, 孙力, 申晓慧, 等. 多年生黑麦草对Pb、Cd胁迫的响应及富集能力研究[J]. 草业学报, 2016, 25(1): 153.
[53] Miyake C, Horiguchi S, Makino A, et al. Effects of light intensity on cyclic electron flow around psi and its relationship to non-photochemical quenching of chl fluorescence in tobacco leaves[J]. Plant Cell Physiol, 2005, 46(11):1819.
[54] 石岱龙, 田武英, 焦青松,等. 外源ATP对NaCl胁迫下菜豆叶片叶绿素荧光特性的调节[J]. 广西植物, 2016, 36(9):1087.
[55] Ashraf M, Harris P J C. Photosynthesis under stressful environments: an overview[J]. Photosynthetica, 2013, 51(2):163.
[56] Herrera A, Fernández M D, Taisma M A. Effects of drought on CAM and water relations in plants of Peperomia carnevalii[J]. Ann Bot, 2000, 86(3):511.
[57] Adams W W, Osmond C B, Sharkey T D.Responses of two CAM species to different irradiances during growth and susceptibility to photoinhibition by high light[J].Plant Physiol, 1987, 83(1):213.
[58] Kaiser W M. Effects of water deficit on photosynthetic capacity[J]. Physiol Plantarum, 1987, 71(1):142.
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