番茄幼苗叶片光合作用、PSII电子传递及活性氧对短期高温胁迫的响应
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摘要
以番茄幼苗为试验材料,研究了光合气体交换参数、叶绿素荧光参数及PSII反应中心、PSII核心蛋白编码基因相对表达量和活性氧代谢对不同高温(25、30、35、40℃)胁迫12 h的响应,以期为番茄高温季节栽培提供参考依据。结果表明:随着温度的升高,番茄幼苗叶片光合碳同化能力受到抑制,30、35℃高温胁迫下番茄幼苗叶片光合作用减弱的原因主要为气孔因素,而40℃时则为气孔和非气孔因素共同限制。高温胁迫下番茄幼苗叶片PSII反应中心活性降低,PSII电子传递受阻,PsbA和PsbP基因相对表达量降低,即高温对番茄幼苗叶片的主要作用位点为PSII供体侧放氧复合体(OEC)和PSII受体侧Q_A向Q_B的传递过程,其原因主要与OEC功能的破坏及D1蛋白的降解有关。高温胁迫下PsbP基因相对表达量降低幅度大于PsbA,并且标准化OJIP曲线上0.3 ms处相对可变荧光(V_K)的增加幅度大于2 ms处相对可变荧光(V_J),说明高温胁迫对番茄幼苗PSII供体侧的伤害程度大于受体侧。番茄幼苗叶片在30、35℃高温胁迫12 h并没有诱导过量的活性氧(ROS)产生,这与非光化学淬灭(NPQ)有效淬灭过剩光能有关,而在40℃高温胁迫下番茄幼苗叶片NPQ显著降低,导致叶片中过剩光能(1-qP)/NPQ和ROS大量积累,这是导致光抑制加剧的重要原因。
In this study,the photosynthetic gas exchange parameters,chlorophyll fluorescence parameters,the gene relative expression of PSII core protein and the reactive oxygen species(ROS) metabolism in response to high temperature stress at different high temperature(25 ℃,30 ℃,35 ℃ and 40 ℃) for 12 hours were studied.The results showed that photosynthetic carbon assimilation ability was inhibited with the increase of temperature in tomato seedlings.The inhibited reason for photosynthesis in tomato seedlings under 30 ℃ and 35 ℃ high temperature stress was stomatal factor,while stomatal and non-stomatal factors were limited collectively at 40 ℃.Under high temperature stress,the activity of PSII reaction center in tomato seedling leaves decreased,PSII electron transport was blocked,and the relative expression of PsbA and PsbP genes decreased,which implied that the main action site in response to high temperature was PSII donor side oxygen release complex(OEC) and the transmission process from Q_A to Q_B on the PSII receptor side in tomato seedling leaves.The relative expression of PsbP gene was significantly higher than that of PsbA under high temperature stress,and the relative variable fluorescence(V_K) at 0.3 ms on the standardized OJIP curve was greater than the relative variable fluorescence(V_J) at 2 ms,indicating that the of damage caused by high temperature stress on the donor side was greater than the receptor side on tomato seedlings.Tomato seedling leaves did not induce excessive production of reactive oxygen species(ROS) at high temperature stress of 30 ℃ and 35 ℃ for 12 hours,which was related to the non-photochemical quenching(NPQ) effective quenching of excess light energy,while NPQ was significantly reduced under 40 ℃ stress,which resulted in excessive accumulation of excess light energy(1-qP)/NPQ and ROS in the leaves.This was an important reason caused further photoinhibition.
In this study,the photosynthetic gas exchange parameters,chlorophyll fluorescence parameters,the gene relative expression of PSII core protein and the reactive oxygen species(ROS) metabolism in response to high temperature stress at different high temperature(25 ℃,30 ℃,35 ℃ and 40 ℃) for 12 hours were studied.The results showed that photosynthetic carbon assimilation ability was inhibited with the increase of temperature in tomato seedlings.The inhibited reason for photosynthesis in tomato seedlings under 30 ℃ and 35 ℃ high temperature stress was stomatal factor,while stomatal and non-stomatal factors were limited collectively at 40 ℃.Under high temperature stress,the activity of PSII reaction center in tomato seedling leaves decreased,PSII electron transport was blocked,and the relative expression of PsbA and PsbP genes decreased,which implied that the main action site in response to high temperature was PSII donor side oxygen release complex(OEC) and the transmission process from Q_A to Q_B on the PSII receptor side in tomato seedling leaves.The relative expression of PsbP gene was significantly higher than that of PsbA under high temperature stress,and the relative variable fluorescence(V_K) at 0.3 ms on the standardized OJIP curve was greater than the relative variable fluorescence(V_J) at 2 ms,indicating that the of damage caused by high temperature stress on the donor side was greater than the receptor side on tomato seedlings.Tomato seedling leaves did not induce excessive production of reactive oxygen species(ROS) at high temperature stress of 30 ℃ and 35 ℃ for 12 hours,which was related to the non-photochemical quenching(NPQ) effective quenching of excess light energy,while NPQ was significantly reduced under 40 ℃ stress,which resulted in excessive accumulation of excess light energy(1-qP)/NPQ and ROS in the leaves.This was an important reason caused further photoinhibition.
引文
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[24] ALEXIEVA V,SERGIEV I,MAPELLI S,et al.The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat[J].Plant,Cell & Environment,2001(24):1337-1344.
[25] LU T,MENG Z,ZHANG G,et al.Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.)[J].Frontiers in Plant Science,2017(18):365.
[26] SUN X,DU Z,REN J,et al.Association of SSR markers with functional traits from heat stress in diverse tall fescue accessions[J].BMC Plant Biology,2015,15(1):116.
[27] DING H,HE J,WU Y,et al.The tomato mitogen-activated protein kinase SlMPK1 is as a negative regulator of the high temperature stress response[J].Plant Physiology,2018,177(2):663-651.
[28] SHARKEY T D,BERNACCHI C J,FARQUHAR G D,et al.Fitting photosynthetic carbon dioxide response curves for C3 leaves[J].Plant Cell Environ,2007(30):1035-1040.
[29] 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].Journal of Experimental Botany,1998,49(327):1715-1721.
[30] STRASSER R J,SRIVASTAVA A,GOVINDJE E.Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria[J].Photochemistry & Photobiology,1995,61(1):32-42.
[31] LI X P,BJORKMAN O,SHI C,et al.A pigment-binding protein essential for regulation of photosynthetic light harvesting[J].Nature,2000,403:391-395.
[32] ZHANG Z S,LI G,GAO H Y,et al.Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L.inbred lines[J].PLoS One,2012,7(8):e42936.
[33] CHEN K,ZHANG M,ZHU H,et al.Ascorbic acid alleviates damage from heat stress in the photosystem II of tall fescue in both the photochemical and thermal phases[J].Frontiers in Plant Science,2017(8):1373.
[34] ZHANG HH,XU N,SUI X,et al.Photosynthesis response to drought stress in leaves of two alfalfa (Medicago sativa) varieties[J].International Journal of Agriculture and Biology,2018,20(5):1012-1020.
[35] ERINLE K O,JIANG Z,MA B,et al.Exogenous calcium induces tolerance to atrazine stress in Pennisetum seedlings and promotes photosynthetic activity,antioxidant enzymes and psbA gene transcripts[J].Ecotoxicology & Environmental Safety,2016,132:403-412.
[36] ASADA M,NISHIMURA T,IFUKU K,et al.Location of the extrinsic subunit PsbP in photosystem II studied by pulsed electron-electron double resonance[J].Biochim Biophys Acta,2018,1859(5):394-399.
[37] BARRA M,HAUMANN M,DAU H.Specific loss of the extrinsic 18 KDa protein from photosystem II upon heating to 47 degrees C causes inactivation of oxygen evolution likely due to Ca release from the Mn-complex[J].Photosynthesis Research,2005,84(1-3):231-237.
[38] JASPERS P,KANGASJ?RVI J.Reactive oxygen species in abiotic stress signaling[J].Physiologia Plantarum,2010,138(4):405.
[39] POSPí?IL P.Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II[J].Biochim Biophys Acta,2012,1817(1):218-231.
[40] BIA?ASEK M,GóRECKA M,MITTLER R,et al.Evidence for the involvement of electrical,calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis[J].Plant & Cell Physiology,2017,58(2):207-215.
[41] DJANAGUIRAMAN M,BOYLE D L,WELTI R,et al.Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation,oxidation,acylation,and damage of organelles[J].BMC Plant Biology,2018,18(1):55.
[42] TAKAHASHI S,NAKAMURA T,SAKAMIZU M,et al.Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals[J].Plant & Cell Physiology,2004,45(2):251-255.
[43] NISHIYAMA Y,ALLAKHVERDIEV S I,MURATA N.Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II[J].Physiologia Plantarum,2011,142(1):35-46.
[44] ESSEMINE J,GOVINDACHARY S,AMMAR S,et al.Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis[J].Environmental & Experimental Botany,2012,80(80):16-26.
[45] TóTH S Z,SCHANSKER G,KISSIMON J,et al.Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.)[J].Journal of Plant Physiology,2005,162(2):181-194.
[2] MITTLER R.ROS and redox signaling in the response of plants to abiotic stress[J].Plant Cell & Environment,2012,35(2):259-270.
[3] XU C,HUANG B.Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance[J].Journal of Experimental Botany,2008,59(15):4183-4194.
[4] LIU G T,LING M,WEI D,et al.Differential proteomic analysis of grapevine leaves by iTRAQ reveals responses to heat stress and subsequent recovery[J].BMC Plant Biology,2014,14(1):110.
[5] YANG Y,CHEN J,LIU Q,et al.Comparative proteomic analysis of the thermotolerant plant Portulaca oleracea acclimation to combined high temperature and humidity stress[J].Journal of Proteome Research,2012,11(7):3605.
[6] REDDY A S N,ALI G S,CELESNIK H,et al.Coping with stresses:Roles of calcium-and calcium/calmodulin-regulated gene expression[J].Plant Cell,2011,23(6):2010.
[7] ALLAKHVERDIEV S I,KRESLAVSKI V D,KLIMOV V V,et al.Heat stress:An overview of molecular responses in photosynthesis[J].Photosynthesis Research,2008,98(1-3):541.
[8] MEHTA P,JAJOO A,MATHUR S,et al.Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves[J].Plant Physiol Biochem,2010,48(1):16-20.
[9] BRESTIC M,ZIVCAK M,KALAJI H M,et al.Photosystem II thermostability in situ:Environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L[J].Plant Physiology & Biochemistry,2012,57(8):93-105.
[10] OUKARROUM A,EL M S,STRASSER R J.Differential heat sensitivity index in barley cultivars (Hordeum vulgare L.) monitored by chlorophyll a fluorescence OKJIP[J].Plant Physiol Biochem,2016,105:102-108.
[11] ROCCO M,ARENA S,RENZONE G,et al.Proteomic analysis of temperature stress-responsive proteins in Arabidopsis thaliana rosette leaves[J].Molecular Biosystems,2013,9(6):1257-1267.
[12] ZHANG M,LI G,HUANG W,et al.Erratum:Proteomic study of Carissa spinarum in response to combined heat and drought stress[J].Proteomics,2010,11(8):1555.
[13] URBAN O,HLAVáOVá M,KLEM K,et al.Combined effects of drought and high temperature on photosynthetic characteristics in four winter wheat genotypes[J].Field Crops Research,2018,223:137-149.
[14] 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].Journal of Experimental Botany,1998,49(327):1715-1721.
[15] HALDIMANN P,FELLER U.Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves[J].Plant Cell & Environment,2005(28):302-317.
[16] ESSEMINE J,GOVINDACHARY S,AMMAR S,et al.Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis[J].Environmental & Experimental Botany,2012,80(3):16-26.
[17] NISHIYAMA Y,ALLAKHVERDIEV S I,MURATA N.Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II[J].Physiologia Plantarum,2011,142(1):35-46.
[18] R?TH S,MIRUS O,BUBLAK D,et al.DNA-binding and repressor function are prerequisite for the turnover of the tomato heat stress transcription factor HsfB1[J].Plant Journal,2016,89(1):31-44.
[19] XU N,ZHANG H H,ZHONG H X,et al.The response of photosynthetic functions of F1 cutting seedlings from Physocarpus amurensis Maxim (♀) × Physocarpus opulifolius “Diabolo” (♂) and the parental leaves to salt stress[J].Frontiers in Plant Science,2018(9):714.
[20] ZHANG L T,GAO H Y,ZHANG Z S,et al.Multiple effects of inhibition of mitochondrial alternative oxidase pathway on photosynthetic apparatus in Rumex K-1 leaves[J].Biologia Plantarum,2012,56:365-368.
[21] STRASSER R J,SRIVASTAVA A,GOVINDJEE.Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria[J].Photochemistry and Photobiology,1995,61(1):32-42.
[22] LIVAK K J,SCHMITTGEN T D.Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method[J].Methods,2001(25):402-408.
[23] ZHANG C G,LEUNG K K,WONG Y S,et al.Germination,growth and physiological responses of mangrove plant (Bruguiera gymnorrhiza) to lubricating oil pollution[J].Environmental and Experimental Botany,2007,60:127-136.
[24] ALEXIEVA V,SERGIEV I,MAPELLI S,et al.The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat[J].Plant,Cell & Environment,2001(24):1337-1344.
[25] LU T,MENG Z,ZHANG G,et al.Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.)[J].Frontiers in Plant Science,2017(18):365.
[26] SUN X,DU Z,REN J,et al.Association of SSR markers with functional traits from heat stress in diverse tall fescue accessions[J].BMC Plant Biology,2015,15(1):116.
[27] DING H,HE J,WU Y,et al.The tomato mitogen-activated protein kinase SlMPK1 is as a negative regulator of the high temperature stress response[J].Plant Physiology,2018,177(2):663-651.
[28] SHARKEY T D,BERNACCHI C J,FARQUHAR G D,et al.Fitting photosynthetic carbon dioxide response curves for C3 leaves[J].Plant Cell Environ,2007(30):1035-1040.
[29] 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].Journal of Experimental Botany,1998,49(327):1715-1721.
[30] STRASSER R J,SRIVASTAVA A,GOVINDJE E.Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria[J].Photochemistry & Photobiology,1995,61(1):32-42.
[31] LI X P,BJORKMAN O,SHI C,et al.A pigment-binding protein essential for regulation of photosynthetic light harvesting[J].Nature,2000,403:391-395.
[32] ZHANG Z S,LI G,GAO H Y,et al.Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L.inbred lines[J].PLoS One,2012,7(8):e42936.
[33] CHEN K,ZHANG M,ZHU H,et al.Ascorbic acid alleviates damage from heat stress in the photosystem II of tall fescue in both the photochemical and thermal phases[J].Frontiers in Plant Science,2017(8):1373.
[34] ZHANG HH,XU N,SUI X,et al.Photosynthesis response to drought stress in leaves of two alfalfa (Medicago sativa) varieties[J].International Journal of Agriculture and Biology,2018,20(5):1012-1020.
[35] ERINLE K O,JIANG Z,MA B,et al.Exogenous calcium induces tolerance to atrazine stress in Pennisetum seedlings and promotes photosynthetic activity,antioxidant enzymes and psbA gene transcripts[J].Ecotoxicology & Environmental Safety,2016,132:403-412.
[36] ASADA M,NISHIMURA T,IFUKU K,et al.Location of the extrinsic subunit PsbP in photosystem II studied by pulsed electron-electron double resonance[J].Biochim Biophys Acta,2018,1859(5):394-399.
[37] BARRA M,HAUMANN M,DAU H.Specific loss of the extrinsic 18 KDa protein from photosystem II upon heating to 47 degrees C causes inactivation of oxygen evolution likely due to Ca release from the Mn-complex[J].Photosynthesis Research,2005,84(1-3):231-237.
[38] JASPERS P,KANGASJ?RVI J.Reactive oxygen species in abiotic stress signaling[J].Physiologia Plantarum,2010,138(4):405.
[39] POSPí?IL P.Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II[J].Biochim Biophys Acta,2012,1817(1):218-231.
[40] BIA?ASEK M,GóRECKA M,MITTLER R,et al.Evidence for the involvement of electrical,calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis[J].Plant & Cell Physiology,2017,58(2):207-215.
[41] DJANAGUIRAMAN M,BOYLE D L,WELTI R,et al.Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation,oxidation,acylation,and damage of organelles[J].BMC Plant Biology,2018,18(1):55.
[42] TAKAHASHI S,NAKAMURA T,SAKAMIZU M,et al.Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals[J].Plant & Cell Physiology,2004,45(2):251-255.
[43] NISHIYAMA Y,ALLAKHVERDIEV S I,MURATA N.Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II[J].Physiologia Plantarum,2011,142(1):35-46.
[44] ESSEMINE J,GOVINDACHARY S,AMMAR S,et al.Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis[J].Environmental & Experimental Botany,2012,80(80):16-26.
[45] TóTH S Z,SCHANSKER G,KISSIMON J,et al.Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.)[J].Journal of Plant Physiology,2005,162(2):181-194.