γ-氨基丁酸对高温胁迫下黑麦草光合特性及碳水化合物代谢的影响
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摘要
以热敏感品种顶峰(Pinnacle)为试验材料,研究了热胁迫下(35℃/30℃,昼/夜)施用外源γ-氨基丁酸(GABA)对黑麦草生长、光合及叶绿素荧光特性、碳水化合物含量及其代谢关键酶基因表达的影响。结果表明,热胁迫造成黑麦草生长减弱,膜透性增加,光合色素含量下降,光合能力和碳水化合物含量显著降低,糖代谢关键酶(蔗糖合成酶、蔗糖磷酸合成酶和转化酶)基因在短时间内(5d)表达显著上调,随后下降;外源施用GABA显著缓解了高温对黑麦草生长的抑制作用,提高了高温胁迫下光合色素和碳水化合物含量,净光合速率(Pn)、气孔导率(Gs)、蒸腾速率(Tr)、CO2羧化效率(CE)、最大光合速率(Amax)和光化学效率(Fv/Fm)、Rubisco最大羧化速率(Vcmax)和RuBP再生速率(Jmax)、光化学猝灭系数(qP)、电子传递速率(ETR)和PSⅡ实际光化学效率(ΦPSⅡ)显著升高,而气孔限制值(Ls)、CO2补偿点(CP)和非光化学猝灭系数(NPQ)显著降低。施用外源GABA降低了高温胁迫下叶片气孔和非气孔限制值,缓解了高温对叶片PSⅡ反应中心的抑制,增强了糖代谢关键酶基因表达的水平,提高了碳水化合物含量,因此有效的提高了黑麦草的耐高温能力。
The aim of this research was to elucidate the effects of exogenousγ-aminobutyric acid(GABA)on high temperature stress metabolism,plant growth,photosynthetic and chlorophyll fluorescence characteristics,carbohydrate content and gene expression levels of key enzymes associated with sugar metabolism.The material studied was a heat sensitive cultivar(Pinnacle)of perennial ryegrass(Lolium perenne)under high temperatures(35/30℃light/dark)in growth chambers for 15 d.It was found that heat stress inhibited plant growth,increased leaf electrolyte leakage and decreased carbohydrate and chlorophyll content,photosynthesis rate.The gene expression levels of key enzymes associated with sugar metabolism were initially up-regulated and subsequently decreased under heat stress.Exogenously applied GABA significantly alleviated the damage effect of heat stress on plant growth and enhanced the chlorophyll content and carbohydrate content under high temperature.The leaf net photosynthetic rate(Pn),stomatal conductance(Gs),transpiration rate(Tr),carboxylation efficiency(CE),maximum assimilation(Amax),photochemical efficiency(Fv/Fm),maximum velocity of carboxylation(Vcmax),maximum electron transfer rate(Jmax),photochemical quenching(qP),electron transport rate(ETR)and actual photochemical efficiency of PSII(ΦPSⅡ)significantly increased while leaf stomatal limitation(Ls),compensation point(CP)and none photochemical quenching(NPQ)significantly decreased after application of GABA under heat stress.To summarize,exogenous application of GABA reduced leaf stomatal and non-stomatal limitations to photosynthesis and alleviated the inhibition of PSII reaction centers,leading to an enhancement in light and dark reactions of photosynthesis and in photosynthetic potential.Expression levels of key genes for sugar metabolism were also enhanced.These physiological changes acted cumulatively to confer a higher tolerance to heat stress in perennial ryegrass.
The aim of this research was to elucidate the effects of exogenousγ-aminobutyric acid(GABA)on high temperature stress metabolism,plant growth,photosynthetic and chlorophyll fluorescence characteristics,carbohydrate content and gene expression levels of key enzymes associated with sugar metabolism.The material studied was a heat sensitive cultivar(Pinnacle)of perennial ryegrass(Lolium perenne)under high temperatures(35/30℃light/dark)in growth chambers for 15 d.It was found that heat stress inhibited plant growth,increased leaf electrolyte leakage and decreased carbohydrate and chlorophyll content,photosynthesis rate.The gene expression levels of key enzymes associated with sugar metabolism were initially up-regulated and subsequently decreased under heat stress.Exogenously applied GABA significantly alleviated the damage effect of heat stress on plant growth and enhanced the chlorophyll content and carbohydrate content under high temperature.The leaf net photosynthetic rate(Pn),stomatal conductance(Gs),transpiration rate(Tr),carboxylation efficiency(CE),maximum assimilation(Amax),photochemical efficiency(Fv/Fm),maximum velocity of carboxylation(Vcmax),maximum electron transfer rate(Jmax),photochemical quenching(qP),electron transport rate(ETR)and actual photochemical efficiency of PSII(ΦPSⅡ)significantly increased while leaf stomatal limitation(Ls),compensation point(CP)and none photochemical quenching(NPQ)significantly decreased after application of GABA under heat stress.To summarize,exogenous application of GABA reduced leaf stomatal and non-stomatal limitations to photosynthesis and alleviated the inhibition of PSII reaction centers,leading to an enhancement in light and dark reactions of photosynthesis and in photosynthetic potential.Expression levels of key genes for sugar metabolism were also enhanced.These physiological changes acted cumulatively to confer a higher tolerance to heat stress in perennial ryegrass.
引文
[1] Xu S,He X Y,Chen W,et al.Effects of heat acclimation on high-temperature stress resistance and heat-tolerance mechanism of Festuca arundinacea and Lolium perenne.Actaecologica Sinica,2006,28(1):162-171.徐胜,何兴元,陈玮,等.热锻炼对高羊茅(Festuca arundinacea)和多年生黑麦草(Lolium perenne)抗高温能力的影响.生态学报,2006,28(1):162-171.
[2] Shi Y H,Wang L Q,Liu J N,et al.Semi-lethal high temperature and heat tolerance of twelve varieties of Lolium perenne.Pratacultural Science,2011,7(2):104-108.石永红,万里强,刘建宁,等.多年生黑麦草高温半致死温度与耐热性研究.草业科学,2011,7(2):104-108.
[3] Ghannoum O,Phillips N G,Sears M A,et al.Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric[CO2]and temperature.Plant Cell and Environment,2010,33(10):1671-1681.
[4] Tang T,Zheng G W,Li W Q.Defense mechanisms of plants photosystem to heat stress.Chinese Journal of Biochemistry and Molecular Biology,2012,28(2):127-132.唐婷,郑国伟,李唯奇.植物光合系统对高温胁迫的响应机制.中国生物化学与分子生物学报,2012,28(2):127-132.
[5] Morvan-Bertrand A,Boucaud J,Le Saos J,et al.Roles of the fructans from leaf sheaths and from the elongating leaf bases in the re-growth following defoliation of Lolium perenne L.Planta,2001,213(1):109-120.
[6] Wang H B,Cui S M,Wang M X,et al.Effects of high temperature on greenhouse cucumber photosynthetic efficiency under CO2enrichment.Journal of Inner Mongolia Agricultural University(Natural Science Edition),2007,28(2):114-118.王红彬,崔世茂,王明喜,等.CO2施肥条件下高温对温室黄瓜光合性能的影响.内蒙古农业大学学报,2007,28(2):114-118.
[7] Lafta A M,Lorenzen J H.Effect of high temperature on plant growth and carbohydrate metabolism in potato.Plant Physiology,1995,109:637-643.
[8] Ge S,Goh E L,Sailor K A,et al.GABA regulates synaptic integration of newly generated neurons in the adult brain.Nature,2006,439(7076):589-593.
[9] Yang Z W,Wang L H,Zhu L,et al.Research on the mechanism of Gamma-aminobutyric acid shunt in plant response to adversity stresses.Current Biotechnology,2014,4(2):77-84.杨泽伟,王龙海,朱莉,等.γ-氨基丁酸代谢旁路在植物响应逆境胁迫中的作用机制研究.生物技术进展,2014,4(2):77-84.
[10] Shelp B J,Bown A W,McLean M D.Metabolism and functions of gamma-aminobutyric acid.Trends in Plant Science,1999,4(11):446-452.
[11] Luo H Y,Gao H B,Xia Q P,et al.Effects of exogenous GABA on reactive oxygen species metabolism and chlorophyll fluorescence parameters in tomato under NaCl stress.Scientia Agricultura Sinica,2011,44(4):753-761.罗黄颖,高洪波,夏庆平,等.γ-氨基丁酸对盐胁迫下番茄活性氧代谢及叶绿素荧光参数的影响.中国农业科学,2011,44(4):753-761.
[12] Gao H B,Zhang T J,LüG Y,et al.Effects of exogenousγ-aminobutyric acid on growth and reactive oxygen species metabolism of cucumber seedlings under NaCl stress.Acta Botanica Boreali-Occidentalia Sinica,2007,27(10):2046-2051.高洪波,章铁军,吕桂云,等.NaCl胁迫下外源γ-氨基丁酸对黄瓜幼苗生长和活性氧代谢的影响.西北植物学报,2007,27(10):2046-2051.
[13] Wang X D,Xie B T,Li J M,et al.Effects of exogenous GABA on waterlogged tolerance in wheat seedlings.Acta Agricultura Boreali-Sinica,2010,25(1):155-160.王晓冬,解备涛,李建民,等.外源γ-氨基丁酸(GABA)对小麦苗期耐涝性的影响.华北农学报,2010,25(1):155-160.
[14] Zhang H Y,Cui L N,Dong S T,et al.Physiological role of hot stress-induced GABA accumulation in maize seedlings.Shandong Agricultural Sciences,2011,7:35-37.张华永,崔丽娜,董树亭,等.热胁迫诱导玉米幼苗γ-氨基丁酸积累的生理作用.山东农业科学,2011,7:35-37.
[15] Li J,Dou X Y,Chen Y M,et al.Nitric oxide involved in seed germination of Trifolium repens L.promoted byγ-aminobutyric acid.Plant Physiology Communications,2008,44(6):1071-1074.李杰,窦晓月,车永梅,等.NO参与γ-氨基丁酸促进白三叶种子的萌发过程.植物生理学通讯,2008,44(6):1071-1074.
[16] Huang J.Effects of exogenous GABA on growth of cucumber seedlings under high temperature stress.Changjiang Vegetables,2016,8:73-78.黄娟.高温胁迫下外源GABA对黄瓜幼苗生长的影响.长江蔬菜,2016,8:73-78.
[17] Li Z,Yu J J,Peng Y,et al.Metabolic pathways regulated byγ-aminobutyric acid(GABA)contributing to heat tolerance in creeping bentgrass(Agrostis stolonifera).Scientific Reports,2016,6:30338.
[18] Wang R M,Xiong X Y.Effect of high temperature stress on growth and physiological metabolism in perennial ryegrass.Acta Prataculturae Sinica,2016,25(8):81-90.王日明,熊兴耀.高温胁迫对黑麦草生长及生理代谢的影响.草业学报,2016,25(8):81-90.
[19] Hu L X,Li H Y,Pang H C,et al.Responses of antioxidant gene,protein and enzymes to salinity stress in two genotypes of perennial ryegrass(Lolium perenne)differing in salt tolerance.Journal of Plant Physiology,2012,169:146-156.
[20] Hiscox T D,Israelstam G F.A method for the extraction of chlorophyll from leaf tissues without maceration.Canadian Journal of Botany,1979,57(12):1332-1334.
[21] Hu L X,Wang Z L,Huang B R.Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C3perennial grass species.Physiologia Plantarum,2010,139:93-106.
[22] Wang Z W.Temporal variation of water-soluble carbohydrate in the rhizome clonal grass Leymus Chinese in response to defoliation.Journal of Ecology,2007,31(4):673-679.王正文.根茎克隆植物羊草体内可溶性碳水化合物的时间变异及其对去叶干扰的响应.植物生态学报,2007,31(4):673-679.
[23] Hu T,Hu L X,Zhang X,et al.Differential responses of CO2assimilation,carbohydrate allocation and gene expression to NaCl stress in perennial ryegrass with different salt tolerance.PloS One,2013,8(6):e66090.
[24] Deng L,Wang Y,Li J L.Effects of different hormones levels on physiological and ecological indicators of Festuca arundinacea cv.Barlexas under heat stress.Grassland and Turf,2010,30(3):33-38.邓蕾,王艳,李建龙.高温胁迫下不同激素处理对高羊茅生理生态指标及耐热性的影响.草原与草坪,2010,30(3):33-38.
[25] Liang Y Y,Wu X L,Li J R,et al.Effects of exogenous GABA on reactive oxygen species metabolism and photosynthesis characteristics of tomatoes under mixed NaCl and NaHCO3stress.Journal of Agricultural University of Hebei,2016,39(3):7-13.梁杨杨,吴晓蕾,李敬蕊,等.盐碱胁迫下对番茄幼苗活性氧代谢及光合性能的影响.河北农业大学学报,2016,39(3):7-13.
[26] Farquhar G D,Von C S,Berry J A.A biochemical model of photosynthetic CO2assimilation in leaves of C3species.Planta,1980,149(1):78-90.
[27] Zhu L,Li X Q,Jia X L,et al.Effect of high temperature stress on photosynthesis in Festuca arundinacea.Journal of Zhejiang Forestry College,2009,26(5):652-655.朱澜,李雪芹,贾晓琳,等.高温胁迫对高羊茅光合作用的影响.浙江林学院学报,2009,26(5):652-655.
[28] Sun K X,Yang S,Guo F,et al.Effects of exogenous calcium on photosynthetic chracteristics of sweet pepper(Capsicum fructescens L.)seedlings.Plant Physiology Journal,2015,51(3):280-286.孙克香,杨莎,郭峰,等.高温强光胁迫下外源钙对甜椒(Capsicum fructescens L.)幼苗光合生理特性的影响.植物生理学报,2015,51(3):280-286.
[29] Xiang L X,Hu L P,Hu X H,et al.Response of reactive oxygen metabolism in melon chloroplasts to short-term salinity-alkalinity stress.Chinese Journal of Applied Ecology,2015,26(12):3746-3752.向丽霞,胡立盼,胡晓辉,等.外源γ-氨基丁酸调控甜瓜叶绿体活性氧代谢应对短期盐碱胁迫.应用生态学报,2015,26(12):3746-3752.
[30] Huang J,Li X F,Huang S,et al.Effects of GABA soaking on cucumber seed germination and seedling growth under different temperature stress.Journal of ChangJiang Vegetables,2014,12:30-35.黄娟,李兴发,黄山,等.γ-氨基丁酸浸种对不同温度胁迫下黄瓜种子萌发和幼苗生长的影响.长江蔬菜,2014,12:30-35.
[31] And G H K,Weis E.Chlorophyll fluorescence and photosynthesis:The Basics.Annual Review of Plant Physiology,2003,42(42):313-349.
[32] Zhang S R.A discussion of chlorophyll fluorescence kinetics parameter and their significance.Chinese Bulletin of Botany,1999,16(4):444-448.张守仁.叶绿素荧光动力学参数的意义及讨论.植物学通报,1999,16(4):444-448.
[33] Li N,Sun T,Mao Z J.Effects of long-term high-temperature stress on the biomass and non-structure carbohydrates of Pinus sylvestris var.mongolicaseedlings.Bulletin of Botanical Research,2014,34(2):212-218.李娜,孙涛,毛子军.长期极端高温胁迫对樟子松幼苗生物量及非结构性碳水化合物的影响.植物研究,2014,34(2):212-218.
[34] Lu S Y,Guo Z F.Physiological responses of turfgrass to abiotic stresses.Acta Prataculturae Sinica,2003,12(4):7-13.卢少云,郭振飞.草坪草逆境生理研究进展.草业学报,2003,12(4):7-13.
[35] Ebrahim M K,Zingsheim O,El-Shourbagy M N,et al.Growth and sugar storage in sugarcane grown at temperatures below and above optimum.Journal of Plant Physiology,1998,153:593-602.
[2] Shi Y H,Wang L Q,Liu J N,et al.Semi-lethal high temperature and heat tolerance of twelve varieties of Lolium perenne.Pratacultural Science,2011,7(2):104-108.石永红,万里强,刘建宁,等.多年生黑麦草高温半致死温度与耐热性研究.草业科学,2011,7(2):104-108.
[3] Ghannoum O,Phillips N G,Sears M A,et al.Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric[CO2]and temperature.Plant Cell and Environment,2010,33(10):1671-1681.
[4] Tang T,Zheng G W,Li W Q.Defense mechanisms of plants photosystem to heat stress.Chinese Journal of Biochemistry and Molecular Biology,2012,28(2):127-132.唐婷,郑国伟,李唯奇.植物光合系统对高温胁迫的响应机制.中国生物化学与分子生物学报,2012,28(2):127-132.
[5] Morvan-Bertrand A,Boucaud J,Le Saos J,et al.Roles of the fructans from leaf sheaths and from the elongating leaf bases in the re-growth following defoliation of Lolium perenne L.Planta,2001,213(1):109-120.
[6] Wang H B,Cui S M,Wang M X,et al.Effects of high temperature on greenhouse cucumber photosynthetic efficiency under CO2enrichment.Journal of Inner Mongolia Agricultural University(Natural Science Edition),2007,28(2):114-118.王红彬,崔世茂,王明喜,等.CO2施肥条件下高温对温室黄瓜光合性能的影响.内蒙古农业大学学报,2007,28(2):114-118.
[7] Lafta A M,Lorenzen J H.Effect of high temperature on plant growth and carbohydrate metabolism in potato.Plant Physiology,1995,109:637-643.
[8] Ge S,Goh E L,Sailor K A,et al.GABA regulates synaptic integration of newly generated neurons in the adult brain.Nature,2006,439(7076):589-593.
[9] Yang Z W,Wang L H,Zhu L,et al.Research on the mechanism of Gamma-aminobutyric acid shunt in plant response to adversity stresses.Current Biotechnology,2014,4(2):77-84.杨泽伟,王龙海,朱莉,等.γ-氨基丁酸代谢旁路在植物响应逆境胁迫中的作用机制研究.生物技术进展,2014,4(2):77-84.
[10] Shelp B J,Bown A W,McLean M D.Metabolism and functions of gamma-aminobutyric acid.Trends in Plant Science,1999,4(11):446-452.
[11] Luo H Y,Gao H B,Xia Q P,et al.Effects of exogenous GABA on reactive oxygen species metabolism and chlorophyll fluorescence parameters in tomato under NaCl stress.Scientia Agricultura Sinica,2011,44(4):753-761.罗黄颖,高洪波,夏庆平,等.γ-氨基丁酸对盐胁迫下番茄活性氧代谢及叶绿素荧光参数的影响.中国农业科学,2011,44(4):753-761.
[12] Gao H B,Zhang T J,LüG Y,et al.Effects of exogenousγ-aminobutyric acid on growth and reactive oxygen species metabolism of cucumber seedlings under NaCl stress.Acta Botanica Boreali-Occidentalia Sinica,2007,27(10):2046-2051.高洪波,章铁军,吕桂云,等.NaCl胁迫下外源γ-氨基丁酸对黄瓜幼苗生长和活性氧代谢的影响.西北植物学报,2007,27(10):2046-2051.
[13] Wang X D,Xie B T,Li J M,et al.Effects of exogenous GABA on waterlogged tolerance in wheat seedlings.Acta Agricultura Boreali-Sinica,2010,25(1):155-160.王晓冬,解备涛,李建民,等.外源γ-氨基丁酸(GABA)对小麦苗期耐涝性的影响.华北农学报,2010,25(1):155-160.
[14] Zhang H Y,Cui L N,Dong S T,et al.Physiological role of hot stress-induced GABA accumulation in maize seedlings.Shandong Agricultural Sciences,2011,7:35-37.张华永,崔丽娜,董树亭,等.热胁迫诱导玉米幼苗γ-氨基丁酸积累的生理作用.山东农业科学,2011,7:35-37.
[15] Li J,Dou X Y,Chen Y M,et al.Nitric oxide involved in seed germination of Trifolium repens L.promoted byγ-aminobutyric acid.Plant Physiology Communications,2008,44(6):1071-1074.李杰,窦晓月,车永梅,等.NO参与γ-氨基丁酸促进白三叶种子的萌发过程.植物生理学通讯,2008,44(6):1071-1074.
[16] Huang J.Effects of exogenous GABA on growth of cucumber seedlings under high temperature stress.Changjiang Vegetables,2016,8:73-78.黄娟.高温胁迫下外源GABA对黄瓜幼苗生长的影响.长江蔬菜,2016,8:73-78.
[17] Li Z,Yu J J,Peng Y,et al.Metabolic pathways regulated byγ-aminobutyric acid(GABA)contributing to heat tolerance in creeping bentgrass(Agrostis stolonifera).Scientific Reports,2016,6:30338.
[18] Wang R M,Xiong X Y.Effect of high temperature stress on growth and physiological metabolism in perennial ryegrass.Acta Prataculturae Sinica,2016,25(8):81-90.王日明,熊兴耀.高温胁迫对黑麦草生长及生理代谢的影响.草业学报,2016,25(8):81-90.
[19] Hu L X,Li H Y,Pang H C,et al.Responses of antioxidant gene,protein and enzymes to salinity stress in two genotypes of perennial ryegrass(Lolium perenne)differing in salt tolerance.Journal of Plant Physiology,2012,169:146-156.
[20] Hiscox T D,Israelstam G F.A method for the extraction of chlorophyll from leaf tissues without maceration.Canadian Journal of Botany,1979,57(12):1332-1334.
[21] Hu L X,Wang Z L,Huang B R.Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C3perennial grass species.Physiologia Plantarum,2010,139:93-106.
[22] Wang Z W.Temporal variation of water-soluble carbohydrate in the rhizome clonal grass Leymus Chinese in response to defoliation.Journal of Ecology,2007,31(4):673-679.王正文.根茎克隆植物羊草体内可溶性碳水化合物的时间变异及其对去叶干扰的响应.植物生态学报,2007,31(4):673-679.
[23] Hu T,Hu L X,Zhang X,et al.Differential responses of CO2assimilation,carbohydrate allocation and gene expression to NaCl stress in perennial ryegrass with different salt tolerance.PloS One,2013,8(6):e66090.
[24] Deng L,Wang Y,Li J L.Effects of different hormones levels on physiological and ecological indicators of Festuca arundinacea cv.Barlexas under heat stress.Grassland and Turf,2010,30(3):33-38.邓蕾,王艳,李建龙.高温胁迫下不同激素处理对高羊茅生理生态指标及耐热性的影响.草原与草坪,2010,30(3):33-38.
[25] Liang Y Y,Wu X L,Li J R,et al.Effects of exogenous GABA on reactive oxygen species metabolism and photosynthesis characteristics of tomatoes under mixed NaCl and NaHCO3stress.Journal of Agricultural University of Hebei,2016,39(3):7-13.梁杨杨,吴晓蕾,李敬蕊,等.盐碱胁迫下对番茄幼苗活性氧代谢及光合性能的影响.河北农业大学学报,2016,39(3):7-13.
[26] Farquhar G D,Von C S,Berry J A.A biochemical model of photosynthetic CO2assimilation in leaves of C3species.Planta,1980,149(1):78-90.
[27] Zhu L,Li X Q,Jia X L,et al.Effect of high temperature stress on photosynthesis in Festuca arundinacea.Journal of Zhejiang Forestry College,2009,26(5):652-655.朱澜,李雪芹,贾晓琳,等.高温胁迫对高羊茅光合作用的影响.浙江林学院学报,2009,26(5):652-655.
[28] Sun K X,Yang S,Guo F,et al.Effects of exogenous calcium on photosynthetic chracteristics of sweet pepper(Capsicum fructescens L.)seedlings.Plant Physiology Journal,2015,51(3):280-286.孙克香,杨莎,郭峰,等.高温强光胁迫下外源钙对甜椒(Capsicum fructescens L.)幼苗光合生理特性的影响.植物生理学报,2015,51(3):280-286.
[29] Xiang L X,Hu L P,Hu X H,et al.Response of reactive oxygen metabolism in melon chloroplasts to short-term salinity-alkalinity stress.Chinese Journal of Applied Ecology,2015,26(12):3746-3752.向丽霞,胡立盼,胡晓辉,等.外源γ-氨基丁酸调控甜瓜叶绿体活性氧代谢应对短期盐碱胁迫.应用生态学报,2015,26(12):3746-3752.
[30] Huang J,Li X F,Huang S,et al.Effects of GABA soaking on cucumber seed germination and seedling growth under different temperature stress.Journal of ChangJiang Vegetables,2014,12:30-35.黄娟,李兴发,黄山,等.γ-氨基丁酸浸种对不同温度胁迫下黄瓜种子萌发和幼苗生长的影响.长江蔬菜,2014,12:30-35.
[31] And G H K,Weis E.Chlorophyll fluorescence and photosynthesis:The Basics.Annual Review of Plant Physiology,2003,42(42):313-349.
[32] Zhang S R.A discussion of chlorophyll fluorescence kinetics parameter and their significance.Chinese Bulletin of Botany,1999,16(4):444-448.张守仁.叶绿素荧光动力学参数的意义及讨论.植物学通报,1999,16(4):444-448.
[33] Li N,Sun T,Mao Z J.Effects of long-term high-temperature stress on the biomass and non-structure carbohydrates of Pinus sylvestris var.mongolicaseedlings.Bulletin of Botanical Research,2014,34(2):212-218.李娜,孙涛,毛子军.长期极端高温胁迫对樟子松幼苗生物量及非结构性碳水化合物的影响.植物研究,2014,34(2):212-218.
[34] Lu S Y,Guo Z F.Physiological responses of turfgrass to abiotic stresses.Acta Prataculturae Sinica,2003,12(4):7-13.卢少云,郭振飞.草坪草逆境生理研究进展.草业学报,2003,12(4):7-13.
[35] Ebrahim M K,Zingsheim O,El-Shourbagy M N,et al.Growth and sugar storage in sugarcane grown at temperatures below and above optimum.Journal of Plant Physiology,1998,153:593-602.