外源一氧化氮对低温下黄瓜幼苗光系统Ⅱ原初光化学反应及光合机构活性的影响
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摘要
采用室内人工模拟低温逆境的方法,研究硝普钠(SNP,NO供体)预处理对低温(昼10℃/夜6℃)胁迫下冷敏感品种‘津研四号’和较耐冷品种‘津优一号’黄瓜(Cucumis sativus)幼苗叶片快速叶绿素荧光动力学曲线及叶绿素荧光参数的影响,探讨了NO对低温胁迫下黄瓜叶片光系统Ⅱ(PSⅡ)原初光化学反应的保护效应,为低温下NO保护黄瓜PSⅡ原初光化学反应的作用机理提供理论依据。结果表明:与‘津研四号’相比,低温对‘津优一号’放氧复合体(OEC)的损伤程度、次级电子受体Q_A的还原速率及电子传递效率的抑制作用更小;NO显著提高了低温胁迫下两品种黄瓜幼苗的最大光化学效率(F_v/F_m)、实际光化学效率(Y_(Ⅱ))、光合电子传递速率(ETR)、光化学淬灭系数(q_P),显著降低了PSⅡ Q_A的氧化还原状态(1-q_P),提高了反应中心捕获的电子传递到Q_A以后的效率(Ψ_o)、反应中心吸收的光能用于电子传递的量子产额(Ψ_(Eo))、光系统I(PSI)末端电子受体的还原能力(Ψ_(Ro))、反应中心密度(RC/CS_o)、PSⅡ叶绿素分子作为反应中心起作用的概率(γ_(RC))、光合性能指数(PI_(ABS)),降低了单位反应中心的光能吸收(ABS/RC)、单位反应中心的热能量耗散(DI_o/RC)、反应中心最大关闭速率(M_o)、单位反应中心的能量传递(ET_o/RC)、K相占J相的相对可变荧光(W_k)及低温24 h后‘津优一号’的J相可变荧光(V_j)、I相可变荧光(V_i)。说明低温胁迫下,外源NO能够有效保护黄瓜幼苗OEC,提高Q_A向次级电子受体Q_B的电子传递速率及质体醌(PQ)接受电子的能力,使Q_A快速进入氧化状态,促进电子传递顺利进行,且NO对‘津优一号’的作用更为显著。
The effect of sodium nitroprusside(SNP,a donor of NO)pretreatment on rapid chlorophyll fluorescence kinetic curves and chlorophyll fluorescence parameters of cucumber(Cucumis sativus)cold-sensitive cultivar‘Jinyan No.4’and cold-tolerant cultivar‘Jingyou No.1’seedlings under chilling(10℃/6℃,day/night)stress was studied.The protective effect of nitric oxide(NO)on the primary photochemical reaction of photosystem Ⅱ(PSⅡ)in cucumber leaves under chilling stress was discussed,providing a theoretical basis for the mechanism of NO protecting PSⅡ primary photochemical reaction of cucumber at chilling stress.The results show that compare to‘Jinyan No.4’,there is less inhibition on the degree of damage of oxygen decomposition complex(OEC),the reduction rate of secondary electron acceptor Q_A and the inhibition of electron transport efficiency on‘Jinyou No.1’.Pretreating with SNP of cucumber before chilling stress could significantly increase maximal photochemical efficiency(F_v/F_m),actual photochemical efficiency(Y_(Ⅱ)),photosynthetic electron transport rate(ETR)and photochemical quenching coefficient(q_P),significantly reduced the redox state of Q_A(1-q_P),improved probability that a trapped exciton moves an electron into the electron transport chain beyond Q_A(Ψ_o),quantum yield for electron transport from Q_A to plastoquinone(Ψ_(Eo)),quantum yield for reduction of end electron acceptors at the PSI acceptor side(Ψ_(Ro)),density of active PSⅡ reaction centers(RC/CS_o),probability that PSⅡ chlorophyll molecule functions as RC(γ_(RC))and performance index of PSⅡ based on absorption(PI_(ABS)),and reduced absorption flux per RC corresponding directly to its apparent antenna size-ratio between chlorophyll in antenna and chlorophyll in RC(ABS/RC),dissipated energy flux per RC at the initial moment of the measurement(DI_o/RC),approximated initial slope of the fluorescent transient(M_o),electron transport flux from Q_A to plastoquinone per RC(ET_o/RC),K-phase accounts for the relative variable fluorescence of J-phase(W_k)and relatively variable fluorescence of J-phase(V_j)and I-phase(V_i)of‘Jinyou No.1’under chilling stress for 24h.It indicates that exogenous NO can effectively protect the oxygen release complex(OEC)in cucumber seedlings,and improve the electron transfer rate of Q_A to Q_B and the ability of plastoquinone to accept electrons.In consequence,Q_A can quickly enter the oxidation state and promote the smooth transfer of electrons.The effect of NO on‘Jinyou No.1’is more significant.
The effect of sodium nitroprusside(SNP,a donor of NO)pretreatment on rapid chlorophyll fluorescence kinetic curves and chlorophyll fluorescence parameters of cucumber(Cucumis sativus)cold-sensitive cultivar‘Jinyan No.4’and cold-tolerant cultivar‘Jingyou No.1’seedlings under chilling(10℃/6℃,day/night)stress was studied.The protective effect of nitric oxide(NO)on the primary photochemical reaction of photosystem Ⅱ(PSⅡ)in cucumber leaves under chilling stress was discussed,providing a theoretical basis for the mechanism of NO protecting PSⅡ primary photochemical reaction of cucumber at chilling stress.The results show that compare to‘Jinyan No.4’,there is less inhibition on the degree of damage of oxygen decomposition complex(OEC),the reduction rate of secondary electron acceptor Q_A and the inhibition of electron transport efficiency on‘Jinyou No.1’.Pretreating with SNP of cucumber before chilling stress could significantly increase maximal photochemical efficiency(F_v/F_m),actual photochemical efficiency(Y_(Ⅱ)),photosynthetic electron transport rate(ETR)and photochemical quenching coefficient(q_P),significantly reduced the redox state of Q_A(1-q_P),improved probability that a trapped exciton moves an electron into the electron transport chain beyond Q_A(Ψ_o),quantum yield for electron transport from Q_A to plastoquinone(Ψ_(Eo)),quantum yield for reduction of end electron acceptors at the PSI acceptor side(Ψ_(Ro)),density of active PSⅡ reaction centers(RC/CS_o),probability that PSⅡ chlorophyll molecule functions as RC(γ_(RC))and performance index of PSⅡ based on absorption(PI_(ABS)),and reduced absorption flux per RC corresponding directly to its apparent antenna size-ratio between chlorophyll in antenna and chlorophyll in RC(ABS/RC),dissipated energy flux per RC at the initial moment of the measurement(DI_o/RC),approximated initial slope of the fluorescent transient(M_o),electron transport flux from Q_A to plastoquinone per RC(ET_o/RC),K-phase accounts for the relative variable fluorescence of J-phase(W_k)and relatively variable fluorescence of J-phase(V_j)and I-phase(V_i)of‘Jinyou No.1’under chilling stress for 24h.It indicates that exogenous NO can effectively protect the oxygen release complex(OEC)in cucumber seedlings,and improve the electron transfer rate of Q_A to Q_B and the ability of plastoquinone to accept electrons.In consequence,Q_A can quickly enter the oxidation state and promote the smooth transfer of electrons.The effect of NO on‘Jinyou No.1’is more significant.
引文
Asgher M,Per TS,Masood A,et al(2017).Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress.Environ Sci Pollut Res,24(3):2273-2285
Bilska A,Sowiński P(2010).Closure of plasmodesmata in maize(Zea mays)at low temperature:a new mechanism for inhibition of photosynthesis.Ann Bot,106(5):675-686
Dulai S,Molnár I,Molnár-Láng M(2011).Changes of photosynthetic parameters in wheat/barley introgression lines during salt stress.Acta Biol Szegediensis,55(1):73-75
Fan H,Du C,Xu Y,et al(2014).Exogenous nitric oxide improves chilling tolerance of Chinese cabbage seedlings by affecting antioxidant enzymes in leaves.Hortic Environ Biotechnol,55(3):159-165
Fan HF,Du CX,Zhu ZJ(2011).Effects of exogenous nitric oxide on plant growth,membrane lipid peroxidation and photosynthesis in cucumber seedling leaves under low temperature.Acta Agr Zhejiangensis,23(3):538-542(in Chinese with English abstract)[樊怀福,杜长霞,朱祝军(2011).外源NO对低温胁迫下黄瓜幼苗生长、叶片膜脂过氧化和光合作用的影响.浙江农业学报,23(3):538-542]
Fancy NN,Bahlmann AK,Loake GJ(2017).Nitric oxide function in plant abiotic stress.Plant Cell Environ,40:462-472
Force L,Critchley C,van Rensen JJS(2003).New fluorescence parameters for monitoring photosynthesis in plants.1.The effect of illumination on the fluorescence parameters of the JIP-test.Photosynth Res,78(1):17-33
Hao H,Fan Y,Li S(2017).Effects of cold acclimation on chilling tolerance and leaf ultrastructure in cotton seedlings.Cotton Sci,29(3):268-273(in Chinese with English abstract)[郝辉芳,范月仙,李生泉(2017).低温锻炼对冷胁迫下棉花叶片细胞超微结构的影响.棉花学报,29(3):268-273]
Hao J,Gu F,Zhu J,et al(2016).Low Night temperature affects the phloem ultrastructure of lateral branches and raffinose family oligosaccharide(RFO)accumulation in RFO-transporting plant melon(Cucumis melo L.)during fruit expansion.PLoS ONE,11(8):e0160909
Jian W,Zhang DW,Zhu F,et al(2015).Nitrate reductase-dependent nitric oxide production is required for regulation alternative oxidase pathway involved in the resistance to Cucumber mosaic virus infection in Arabidopsis.Plant Growth Regul,77(1):99-107
Khoshbakht D,Asghari MR,Haghighi M(2018).Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence,photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress.Photosynthetica,56(4):1313-1325
Lazár D(2006).The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light.Funct Plant Biol,33(1):9-30
Liu C,Yuan Y,Gai SP,et al(2014).Effects of strong light coupled with high temperature treatment on energy transfer between PSII and PSI in tree peony leaves.Acta Hortic Sin,41(2):311-318(in Chinese with English abstract)[刘超,袁野,盖树鹏等(2014).强光高温交叉胁迫对牡丹叶片PSII和PSI之间能量传递的影响.园艺学报,41(2):311-318]
Liu QQ,Ma SB,Feng XH,et al(2016).Effects of grafting on the fast chlorophyll fluorescence induction dynamics of pepper seedlings under temperature stress.Acta Hortic Sin,43(5):885-896(in Chinese with English abstract)[刘倩倩,马寿宾,冯希环等(2016).嫁接对高温和低温胁迫下辣椒幼苗快速叶绿素荧光诱导动力学特性的影响.园艺学报,43(5):885-896]
Liu YF,Zhang GX,Qi MF,et al(2015).Effects of calcium on photosynthesis,antioxidant system,and chloroplast ultrastructure in tomato leaves under low night temperature stress.J Plant Growth Regul,34(2):263-273
Mur LAJ,Mandon J,Persijn S,et al(2013).Nitric oxide in plants:an assessment of the current state of knowledge.AoB Plants,5(1):pls052
Murchie EH,Lawson T(2013).Chlorophyll fluorescence analysis:a guide to good practice and understanding some new applications.J Exp Bot,64(13):3983-3998
Paunov M,Koleva L,Vassilev A,et al(2018).Effects of different metals on photosynthesis:cadmium and zinc affect chlorophyll fluorescence in durum wheat.Int J Mol Sci,19(3):787
Puyaubert J,Baudouin E(2014).New clues for a cold case:nitric oxide response to low temperature.Plant Cell Environ,37(12):2623-2630
Schansker G,Srivastava A,Govindiee,et al(2003).Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise(OJIP)in pea leaves.Funct Plant Biol,30(7):785-796
Schansker G,Tóth SZ,Strasser RJ(2004).Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.Biochim Biophys Acta,1706(3):250-261
Shao RX,Li LL,Zheng HF,et al(2016).Effects of exogenous nitric oxide on photosynthesis of maize seedlings under drought stress.Sci Agr Sin,49(2):251-259(in Chinese with English abstract)[邵瑞鑫,李蕾蕾,郑会芳等(2016).外源一氧化氮对干旱胁迫下玉米幼苗光合作用的影响.中国农业科学,49(2):251-259]
Strasser RJ,Srivastava A,Govindjee(1994).Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.Photochem photobiol,61:32-42
Strasser RJ,Tsimilli-Michael M,Srivastava A(2004).Analysis of the chlorophyll a fluorescence transient.In:Papageorgiou GC,Govindjee(eds).Chlorophyll a Fluorescence.Dordrecht:Springer,321-362
van Kooten O,Snel JFH(1990).The use of chlorophyll fluorescence nomenclature in plant stress physiology.Photosynth Res,25(3):147-150
Wang D,Liu Y,Tan X,et al(2015).Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea(L.)Gaud under cadmium stress.Environ Sci Pollut Res,22(5):3489-3497
Wang F,Li YS,Peng YL,et al(2017).Effects of exogenous nitric oxide on low temperature stress of maize seedlings.Agr Res Arid Areas,35(4):270-275(in Chinese with English abstract)[王芳,李永生,彭云玲等(2017).外源一氧化氮对玉米幼苗抗低温胁迫的影响.干旱地区农业研究,35(4):270-275]
Wang LZ,Wang LM,Xiang HT,et al(2016 a).Relationship of photosynthetic efficiency and seed-setting rate in two contrasting rice cultivars under chilling stress.Photosynthetica,54(4):581-588
Wang Z,Cao J,Jiang W(2016 b).Changes in sugar metabolism caused by exogenous oxalic acid related to chilling tolerance of apricot fruit.Postharvest Biol Technol,114:10-16
Yang MS,Wang YF,Gan XX,et al(2012).Effects of exogenous nitric oxide on growth,antioxidant system and photosynthetic characteristics in seedling of cotton cultivar under chilling injury stress.Sci Agr Sin,45(15):3058-3067(in Chinese with English abstract)[杨美森,王雅芳,干秀霞等(2012).外源一氧化氮对冷害胁迫下棉花幼苗生长、抗氧化系统和光合特性的影响.中国农业科学,45(15):3058-3067]
Yang XL,Xu H,Li D,et al(2018).Effect of melatonin priming on photosynthetic capacity of tomato leaves under low-temperature stress.Photosynthetica,56(3):884-892
Zhao MG,Chen L,Zhang LL,et al(2009).Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis.Plant Physiol,151(2):755-767
Zheng YL,Li WQ,Sun WB(2015).Effects of acclimation and pretreatment with abscisic acid or salicylic acid on tolerance of Trigonobalanus doichangensis to extreme temperatures.Biol Plant,59(2):382-388
Bilska A,Sowiński P(2010).Closure of plasmodesmata in maize(Zea mays)at low temperature:a new mechanism for inhibition of photosynthesis.Ann Bot,106(5):675-686
Dulai S,Molnár I,Molnár-Láng M(2011).Changes of photosynthetic parameters in wheat/barley introgression lines during salt stress.Acta Biol Szegediensis,55(1):73-75
Fan H,Du C,Xu Y,et al(2014).Exogenous nitric oxide improves chilling tolerance of Chinese cabbage seedlings by affecting antioxidant enzymes in leaves.Hortic Environ Biotechnol,55(3):159-165
Fan HF,Du CX,Zhu ZJ(2011).Effects of exogenous nitric oxide on plant growth,membrane lipid peroxidation and photosynthesis in cucumber seedling leaves under low temperature.Acta Agr Zhejiangensis,23(3):538-542(in Chinese with English abstract)[樊怀福,杜长霞,朱祝军(2011).外源NO对低温胁迫下黄瓜幼苗生长、叶片膜脂过氧化和光合作用的影响.浙江农业学报,23(3):538-542]
Fancy NN,Bahlmann AK,Loake GJ(2017).Nitric oxide function in plant abiotic stress.Plant Cell Environ,40:462-472
Force L,Critchley C,van Rensen JJS(2003).New fluorescence parameters for monitoring photosynthesis in plants.1.The effect of illumination on the fluorescence parameters of the JIP-test.Photosynth Res,78(1):17-33
Hao H,Fan Y,Li S(2017).Effects of cold acclimation on chilling tolerance and leaf ultrastructure in cotton seedlings.Cotton Sci,29(3):268-273(in Chinese with English abstract)[郝辉芳,范月仙,李生泉(2017).低温锻炼对冷胁迫下棉花叶片细胞超微结构的影响.棉花学报,29(3):268-273]
Hao J,Gu F,Zhu J,et al(2016).Low Night temperature affects the phloem ultrastructure of lateral branches and raffinose family oligosaccharide(RFO)accumulation in RFO-transporting plant melon(Cucumis melo L.)during fruit expansion.PLoS ONE,11(8):e0160909
Jian W,Zhang DW,Zhu F,et al(2015).Nitrate reductase-dependent nitric oxide production is required for regulation alternative oxidase pathway involved in the resistance to Cucumber mosaic virus infection in Arabidopsis.Plant Growth Regul,77(1):99-107
Khoshbakht D,Asghari MR,Haghighi M(2018).Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence,photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress.Photosynthetica,56(4):1313-1325
Lazár D(2006).The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light.Funct Plant Biol,33(1):9-30
Liu C,Yuan Y,Gai SP,et al(2014).Effects of strong light coupled with high temperature treatment on energy transfer between PSII and PSI in tree peony leaves.Acta Hortic Sin,41(2):311-318(in Chinese with English abstract)[刘超,袁野,盖树鹏等(2014).强光高温交叉胁迫对牡丹叶片PSII和PSI之间能量传递的影响.园艺学报,41(2):311-318]
Liu QQ,Ma SB,Feng XH,et al(2016).Effects of grafting on the fast chlorophyll fluorescence induction dynamics of pepper seedlings under temperature stress.Acta Hortic Sin,43(5):885-896(in Chinese with English abstract)[刘倩倩,马寿宾,冯希环等(2016).嫁接对高温和低温胁迫下辣椒幼苗快速叶绿素荧光诱导动力学特性的影响.园艺学报,43(5):885-896]
Liu YF,Zhang GX,Qi MF,et al(2015).Effects of calcium on photosynthesis,antioxidant system,and chloroplast ultrastructure in tomato leaves under low night temperature stress.J Plant Growth Regul,34(2):263-273
Mur LAJ,Mandon J,Persijn S,et al(2013).Nitric oxide in plants:an assessment of the current state of knowledge.AoB Plants,5(1):pls052
Murchie EH,Lawson T(2013).Chlorophyll fluorescence analysis:a guide to good practice and understanding some new applications.J Exp Bot,64(13):3983-3998
Paunov M,Koleva L,Vassilev A,et al(2018).Effects of different metals on photosynthesis:cadmium and zinc affect chlorophyll fluorescence in durum wheat.Int J Mol Sci,19(3):787
Puyaubert J,Baudouin E(2014).New clues for a cold case:nitric oxide response to low temperature.Plant Cell Environ,37(12):2623-2630
Schansker G,Srivastava A,Govindiee,et al(2003).Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise(OJIP)in pea leaves.Funct Plant Biol,30(7):785-796
Schansker G,Tóth SZ,Strasser RJ(2004).Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.Biochim Biophys Acta,1706(3):250-261
Shao RX,Li LL,Zheng HF,et al(2016).Effects of exogenous nitric oxide on photosynthesis of maize seedlings under drought stress.Sci Agr Sin,49(2):251-259(in Chinese with English abstract)[邵瑞鑫,李蕾蕾,郑会芳等(2016).外源一氧化氮对干旱胁迫下玉米幼苗光合作用的影响.中国农业科学,49(2):251-259]
Strasser RJ,Srivastava A,Govindjee(1994).Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.Photochem photobiol,61:32-42
Strasser RJ,Tsimilli-Michael M,Srivastava A(2004).Analysis of the chlorophyll a fluorescence transient.In:Papageorgiou GC,Govindjee(eds).Chlorophyll a Fluorescence.Dordrecht:Springer,321-362
van Kooten O,Snel JFH(1990).The use of chlorophyll fluorescence nomenclature in plant stress physiology.Photosynth Res,25(3):147-150
Wang D,Liu Y,Tan X,et al(2015).Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea(L.)Gaud under cadmium stress.Environ Sci Pollut Res,22(5):3489-3497
Wang F,Li YS,Peng YL,et al(2017).Effects of exogenous nitric oxide on low temperature stress of maize seedlings.Agr Res Arid Areas,35(4):270-275(in Chinese with English abstract)[王芳,李永生,彭云玲等(2017).外源一氧化氮对玉米幼苗抗低温胁迫的影响.干旱地区农业研究,35(4):270-275]
Wang LZ,Wang LM,Xiang HT,et al(2016 a).Relationship of photosynthetic efficiency and seed-setting rate in two contrasting rice cultivars under chilling stress.Photosynthetica,54(4):581-588
Wang Z,Cao J,Jiang W(2016 b).Changes in sugar metabolism caused by exogenous oxalic acid related to chilling tolerance of apricot fruit.Postharvest Biol Technol,114:10-16
Yang MS,Wang YF,Gan XX,et al(2012).Effects of exogenous nitric oxide on growth,antioxidant system and photosynthetic characteristics in seedling of cotton cultivar under chilling injury stress.Sci Agr Sin,45(15):3058-3067(in Chinese with English abstract)[杨美森,王雅芳,干秀霞等(2012).外源一氧化氮对冷害胁迫下棉花幼苗生长、抗氧化系统和光合特性的影响.中国农业科学,45(15):3058-3067]
Yang XL,Xu H,Li D,et al(2018).Effect of melatonin priming on photosynthetic capacity of tomato leaves under low-temperature stress.Photosynthetica,56(3):884-892
Zhao MG,Chen L,Zhang LL,et al(2009).Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis.Plant Physiol,151(2):755-767
Zheng YL,Li WQ,Sun WB(2015).Effects of acclimation and pretreatment with abscisic acid or salicylic acid on tolerance of Trigonobalanus doichangensis to extreme temperatures.Biol Plant,59(2):382-388