镉胁迫对菜豆叶片抗氰呼吸、抗氧化及PSⅡ光合特性的影响
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摘要
为探究镉胁迫下抗氰呼吸(交替途径)对植物体的保护作用和可能存在的作用机制,以菜豆幼苗为研究材料,探讨镉胁迫对菜豆叶片抗氰呼吸、抗氧化和光系统Ⅱ(PSⅡ)光合特性的影响,以及抗氰呼吸对PSⅡ的影响是否与其参与抗氧化调节作用有关.结果显示:随镉处理浓度的增加,菜豆叶片抗氰呼吸能力和抗氧化酶[过氧化氢酶(CAT)、过氧化物酶(POD)、抗坏血酸过氧化物酶(APX)、超氧化物歧化酶(SOD)]活性以及过氧化氢(H_2O_2)含量呈现先升高后降低趋势,而超氧阴离子自由基(O_2~(·-))则逐渐显著上升;同时,菜豆幼苗叶片F_v′/F_m′(光适应下PSⅡ最大光化学效率)、Y(Ⅱ)(PSⅡ实际光化学效率)和qP(光化学淬灭系数)、ETR(PSⅡ光合电子传递速率)下降,而叶片非光化学荧光猝灭系数(NPQ)则上升.非镉胁迫条件下,叶面分别喷施H_2O_2、O_2~(·-)消除剂或抗氰呼吸抑制剂未对上述所测叶绿素荧光参数造成不良影响,且H_2O_2消除剂的施加使得qP和ETR显著提高.在镉胁迫下,叶面分别喷施H_2O_2或O_2~(·-)消除剂有效缓解了镉导致的PSⅡ光化学活性的降低,而抗氰呼吸抑制剂的施加则造成了镉胁迫造成的PSⅡ光化学活性的进一步下降以及H_2O_2和O_2~(·-)含量的进一步提高,并导致了CAT、POD、APX抗氧化酶活性水平的降低.上述研究结果表明,镉胁迫下抗氰呼吸可有效缓解镉胁迫导致的菜豆幼苗叶片活性氧的过量积累和抗氧化酶活性的上升以及PSⅡ光化学活性的下降;且抗氰呼吸对PSⅡ的保护作用可能与其调节抗氧化的功能有关.(图3表2参25)
To explore the protective effects and possible mechanisms of cyanide-resistant respiration(alternating pathway)of plants under cadmium stress, we investigated the effects of cadmium stress on cyanide-resistant respiration, antioxidation,and photosynthetic characteristics of photosystem Ⅱ(PS Ⅱ) in kidney bean leaves. We determined whether the effects of cyanide-resistant respiration on PS Ⅱ is related to its involvement in antioxidant regulation. The results showed that the ability of cyanide-resistant respiration, the activity of antioxidant enzymes [including superoxide dismutase(SOD), catalase(CAT), peroxidase(POD), and ascorbate peroxidase(APX)] and the content of hydrogen peroxide(H_2O_2) first increased but then decreased with the increase in cadmium concentration, whereas the superoxide anion radical(O_2~(·-)) content significantly increased with the increase in cadmium concentrations. Simultaneously, the effective photochemical quantum yield of PS Ⅱ photosynthetic [Y(Ⅱ)], photochemical quenching coefficient(qP), and rate of non-cyclic electron transport through PS Ⅱ(ETR)of the leaves decreased. However, the non-photochemical quenching(NPQ) of leaves increased with the increase in cadmium concentration. Under conditions without cadmium stress, spraying with exogenous eliminator of H_2O_2 and O_2~(·-)or inhibitor of cyanide-resistant respiration on the leaf surface did not adversely affect chlorophyll fluorescence parameters, but qP and ETR significantly increased with the application of H_2O_2 eliminator. Under cadmium stress, treatment with the exogenous eliminator of H_2O_2 and O_2~(·-)could effectively alleviate the decrease in photochemical activity of PS Ⅱ, whereas treatment with the inhibitor of cyanide-resistant respiratory pathway caused further decrease in PS Ⅱ photochemical efficiency, increase in reactive oxygen species level, and decrease in antioxidant enzyme activities. The results showed that cyanide-resistant respiration can effectively alleviate the excessive accumulation of reactive oxygen species, increase of antioxidant enzyme activity, and decrease the PS Ⅱ photochemical activity in the kidney bean seedling leaves caused by cadmium stress. Furthermore, the function of the cyanide-resistant respiratory pathway in protecting the PS Ⅱ from Cd stress could be related to the ability of the cyanide-resistant respiratory pathway to regulate the antioxidant capacity of plants.
To explore the protective effects and possible mechanisms of cyanide-resistant respiration(alternating pathway)of plants under cadmium stress, we investigated the effects of cadmium stress on cyanide-resistant respiration, antioxidation,and photosynthetic characteristics of photosystem Ⅱ(PS Ⅱ) in kidney bean leaves. We determined whether the effects of cyanide-resistant respiration on PS Ⅱ is related to its involvement in antioxidant regulation. The results showed that the ability of cyanide-resistant respiration, the activity of antioxidant enzymes [including superoxide dismutase(SOD), catalase(CAT), peroxidase(POD), and ascorbate peroxidase(APX)] and the content of hydrogen peroxide(H_2O_2) first increased but then decreased with the increase in cadmium concentration, whereas the superoxide anion radical(O_2~(·-)) content significantly increased with the increase in cadmium concentrations. Simultaneously, the effective photochemical quantum yield of PS Ⅱ photosynthetic [Y(Ⅱ)], photochemical quenching coefficient(qP), and rate of non-cyclic electron transport through PS Ⅱ(ETR)of the leaves decreased. However, the non-photochemical quenching(NPQ) of leaves increased with the increase in cadmium concentration. Under conditions without cadmium stress, spraying with exogenous eliminator of H_2O_2 and O_2~(·-)or inhibitor of cyanide-resistant respiration on the leaf surface did not adversely affect chlorophyll fluorescence parameters, but qP and ETR significantly increased with the application of H_2O_2 eliminator. Under cadmium stress, treatment with the exogenous eliminator of H_2O_2 and O_2~(·-)could effectively alleviate the decrease in photochemical activity of PS Ⅱ, whereas treatment with the inhibitor of cyanide-resistant respiratory pathway caused further decrease in PS Ⅱ photochemical efficiency, increase in reactive oxygen species level, and decrease in antioxidant enzyme activities. The results showed that cyanide-resistant respiration can effectively alleviate the excessive accumulation of reactive oxygen species, increase of antioxidant enzyme activity, and decrease the PS Ⅱ photochemical activity in the kidney bean seedling leaves caused by cadmium stress. Furthermore, the function of the cyanide-resistant respiratory pathway in protecting the PS Ⅱ from Cd stress could be related to the ability of the cyanide-resistant respiratory pathway to regulate the antioxidant capacity of plants.
引文
1赛闹汪青,张牡丹,马小俊,冉瑞兰,贾凌云,冯汉青.镉胁迫对黄芪幼苗的生理学影响及凹凸棒粘土对镉胁迫缓解作用的研究[J].中国中药杂志, 2018, 43(15):3115-3126[Sainao WQ, Zhang MD, Ma XJ,Ran RL, Jia L YY, Feng HQ. Physiological effects of cadmium stress on Astragalus membranaceus seedlings and alleviative effects of attapulgite clay on cadmium stress. China J Chin Mat Med, 2018, 43(15):3115-3126]
2 Booth B. The added danger of counterfeit cigarettes[J]. Environ Sci Technol, 2005, 39(2):34A
3 Wan L, Zhang H. Cadmium toxicity[J]. Plant Signal Behav, 2012, 7(3):345-348
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5 李耕,张善平,刘鹏,高辉远,王敬锋,刘晨旭,董树亭,张吉旺.镉对玉米叶片光系统活性的影响[J].中国农业科学, 2011, 44(15):3118-3126[Li G, Zhang S P, Liu P, Gao H Y, Wang J F, Liu C X, Dong S T, Zhang J W. Effect of cadmium on photosystem activities of maize(Zea mays L.)leaves[J]. Sci Agric Sin, 2011, 44(15):3118-3126]
6 徐秀玉,孙山,金立桥,刘美君,高辉远.干旱胁迫下平邑甜茶叶片交替呼吸途径上调对光破坏的防御作用[J].植物生理学报, 2015,51(12):2119-2125[Xu XY, Sun S, Jin LQ, Liu MJ, Gao HY. Upregulation of the mitochondrial alternative oxidase pathway enhances photoprotectioninMalus hupehensisleavesunderdroughtstress[J].J Plant Physiol, 2015, 51(12):2119-2125
7 Mackenzie S, Mcintosh L. Higher plant mitochondria[J]. Plant Cell,1999, 11(4):571-586
8 Padmasree K, Raghavendra AS. Response of photosynthetic carbon assimilationinmesophyllprotoplaststorestrictiononmitochondrial oxidative metabolism:metabolites related to the redox status and sucrose biosynthesis[J]. Photosynth Res, 1999, 62(2):231-239
9 Lis RV, Atteia A. Control of mitochondrial function via photosynthetic redox signals[J]. Photosynth Res, 2004, 79(2):133-148
10 Zhang LT, Cao HY, Zhang ZS, Xue ZC, Meng QW. Multiple effects of inhibition of mitochondrial alternative oxidase pathway on photosynthetic apparatus in Rumex, K-1 leaves[J]. Biol Plant, 2012, 56(2):365-368
11 Demmig-Adams B, Adams WW. Xanthophyll cycle and light stress in nature:uniform response to excess direct sunlight among higher plant species[J]. Planta, 1996, 198(3):460-470
12 李晓,冯伟,曾晓春.叶绿素荧光分析技术及应用进展[J].西北植物学报, 2006, 26(10):2186-2196[Li X, Feng W, Zeng X. Advances in chlorophyll fluorescence analysis and its uses[J]. Acta Bot Bot-Occid Sin, 2006, 26(10):2186-2196]
13 Achary VMM, Panda BB. Aluminium-induced DNA damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates[J]. Mutagenesis, 2010, 25(2):201-209
14 王爱国,罗广华.植物的超氧物自由基与羟胺反应的定量关系[J].植物生理学报, 1990, 26(6):55-57[Wang AG, Luo GH. Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants[J]. J Plant Physiol, 1990, 26(6):55-57]
15 Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y.Interactionofnitricoxideandreactiveoxygenspeciesandassociated regulation of root growth in wheat seedlings under zinc stress[J].Ecotoxicol Environ Saf, 2015, 113(113C):95-102
16 Dhindsa MS. Intraspecific nest parasitism in two species of Indian weaverbirds Ploceus benghalensis and P. manyar[J]. IBIS, 1983, 125(2):243-245
17 曾韶西,王以柔,刘鸿先.低温光照下与黄瓜子叶叶绿素降低有关的酶促反应[J].植物生理学报, 1991, 27(2):177-182[Zeng SX, Wang YR, Liu HX. Some enzymatic reaction to chlorophyll degradation in cucumber cotyledons under chilling in the light[J]. J Plant Physiol,1991, 27(2):177-182]
18 Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts[J]. Plant Cell Physiol, 1981,22(5):867-880
19 M?ller IM, Bérczi A, Plas LHWVD, Lambers H. Measurement of the activity and capacity of the alternative pathway in intact plant tissues:identification of problems and possible solutions[J]. Physiol Plant, 1988,72(3):642-649
20 Feng HQ, Sun K, Wei Y, Wang RF, Jia LY, Zhang JP, Li Y. Role of cyanide-resistant respiration during light-induced attraction of predators to herbivore-infested leaves[J]. Photosythetica, 2013, 51(4):583-592
21 彭金梅,刘国顺,贾方方,周小红,刘典三,何永秋,邢雪霞. Cd胁迫对烤烟生理特性及积累特征的影响[J].江西农业学报, 2013, 25(4):141-146[Peng JM, Liu GS, Jia FF, Zhou XH, Liu DS, He YQ, Xing XX. Effects of cadmium stress on physiological characteristics and accumulation features of flue-cured tobacco[J]. Acta Agric Jiangxi,2013, 25(4):141-146]
22 贺国强,刘茜,郭振楠,付茂辉,李洪亮,刘琳,李恒全,张会慧.镉胁迫对烤烟叶片光合和叶绿素荧光特性的影响[J].华北农学报,2016,31:388-393[He GQ, Liu Q, Guo ZN, Fu MH, Li HL, Liu L,Li HQ, Zhang HH. Effects of cadmium stress on photosynthetic and characteristics, chlorophyll fluorescence in leaves of flue-cured tobacco[J]. Acta Agric Bor-Sin, 2016, 31:388-393]
23 Krause GH, Winter K. Photoinhibition of photosynthesis in plants growing in natural tropical forest gaps:a chlorophyll fluorescence study[J]. Plant Biol, 2015, 109(6):456-462
24 Rehman AU, Cser K, Sass L, Vass I. Characterization of singlet oxygen production and its involvement in photodamage of acclimation of kidney bean(Phaseolus vulgaris). Photosynthetica, 2015, 53(2):195-200
25 吴强,李红玉,张立新,梁厚果.环境胁迫与植物抗氰呼吸[J].西北植物学报, 2003, 23(1):164-170[Wu Q, Li HY, Zhang LX, Liang HG.The stresses and thecyanide-resistant respiration[J].Acta Bot Bor Occid Sin, 2003, 23(1):164-170]
2 Booth B. The added danger of counterfeit cigarettes[J]. Environ Sci Technol, 2005, 39(2):34A
3 Wan L, Zhang H. Cadmium toxicity[J]. Plant Signal Behav, 2012, 7(3):345-348
4 ?ikili Y, Samet H, Dursun S. Cadmium toxicity and its effects on growth andmetalnutrientionaccumulationinSolanaceaeplants[J].Tarim Biliml Derg, 2016, 22(4):576-587
5 李耕,张善平,刘鹏,高辉远,王敬锋,刘晨旭,董树亭,张吉旺.镉对玉米叶片光系统活性的影响[J].中国农业科学, 2011, 44(15):3118-3126[Li G, Zhang S P, Liu P, Gao H Y, Wang J F, Liu C X, Dong S T, Zhang J W. Effect of cadmium on photosystem activities of maize(Zea mays L.)leaves[J]. Sci Agric Sin, 2011, 44(15):3118-3126]
6 徐秀玉,孙山,金立桥,刘美君,高辉远.干旱胁迫下平邑甜茶叶片交替呼吸途径上调对光破坏的防御作用[J].植物生理学报, 2015,51(12):2119-2125[Xu XY, Sun S, Jin LQ, Liu MJ, Gao HY. Upregulation of the mitochondrial alternative oxidase pathway enhances photoprotectioninMalus hupehensisleavesunderdroughtstress[J].J Plant Physiol, 2015, 51(12):2119-2125
7 Mackenzie S, Mcintosh L. Higher plant mitochondria[J]. Plant Cell,1999, 11(4):571-586
8 Padmasree K, Raghavendra AS. Response of photosynthetic carbon assimilationinmesophyllprotoplaststorestrictiononmitochondrial oxidative metabolism:metabolites related to the redox status and sucrose biosynthesis[J]. Photosynth Res, 1999, 62(2):231-239
9 Lis RV, Atteia A. Control of mitochondrial function via photosynthetic redox signals[J]. Photosynth Res, 2004, 79(2):133-148
10 Zhang LT, Cao HY, Zhang ZS, Xue ZC, Meng QW. Multiple effects of inhibition of mitochondrial alternative oxidase pathway on photosynthetic apparatus in Rumex, K-1 leaves[J]. Biol Plant, 2012, 56(2):365-368
11 Demmig-Adams B, Adams WW. Xanthophyll cycle and light stress in nature:uniform response to excess direct sunlight among higher plant species[J]. Planta, 1996, 198(3):460-470
12 李晓,冯伟,曾晓春.叶绿素荧光分析技术及应用进展[J].西北植物学报, 2006, 26(10):2186-2196[Li X, Feng W, Zeng X. Advances in chlorophyll fluorescence analysis and its uses[J]. Acta Bot Bot-Occid Sin, 2006, 26(10):2186-2196]
13 Achary VMM, Panda BB. Aluminium-induced DNA damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates[J]. Mutagenesis, 2010, 25(2):201-209
14 王爱国,罗广华.植物的超氧物自由基与羟胺反应的定量关系[J].植物生理学报, 1990, 26(6):55-57[Wang AG, Luo GH. Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants[J]. J Plant Physiol, 1990, 26(6):55-57]
15 Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y.Interactionofnitricoxideandreactiveoxygenspeciesandassociated regulation of root growth in wheat seedlings under zinc stress[J].Ecotoxicol Environ Saf, 2015, 113(113C):95-102
16 Dhindsa MS. Intraspecific nest parasitism in two species of Indian weaverbirds Ploceus benghalensis and P. manyar[J]. IBIS, 1983, 125(2):243-245
17 曾韶西,王以柔,刘鸿先.低温光照下与黄瓜子叶叶绿素降低有关的酶促反应[J].植物生理学报, 1991, 27(2):177-182[Zeng SX, Wang YR, Liu HX. Some enzymatic reaction to chlorophyll degradation in cucumber cotyledons under chilling in the light[J]. J Plant Physiol,1991, 27(2):177-182]
18 Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts[J]. Plant Cell Physiol, 1981,22(5):867-880
19 M?ller IM, Bérczi A, Plas LHWVD, Lambers H. Measurement of the activity and capacity of the alternative pathway in intact plant tissues:identification of problems and possible solutions[J]. Physiol Plant, 1988,72(3):642-649
20 Feng HQ, Sun K, Wei Y, Wang RF, Jia LY, Zhang JP, Li Y. Role of cyanide-resistant respiration during light-induced attraction of predators to herbivore-infested leaves[J]. Photosythetica, 2013, 51(4):583-592
21 彭金梅,刘国顺,贾方方,周小红,刘典三,何永秋,邢雪霞. Cd胁迫对烤烟生理特性及积累特征的影响[J].江西农业学报, 2013, 25(4):141-146[Peng JM, Liu GS, Jia FF, Zhou XH, Liu DS, He YQ, Xing XX. Effects of cadmium stress on physiological characteristics and accumulation features of flue-cured tobacco[J]. Acta Agric Jiangxi,2013, 25(4):141-146]
22 贺国强,刘茜,郭振楠,付茂辉,李洪亮,刘琳,李恒全,张会慧.镉胁迫对烤烟叶片光合和叶绿素荧光特性的影响[J].华北农学报,2016,31:388-393[He GQ, Liu Q, Guo ZN, Fu MH, Li HL, Liu L,Li HQ, Zhang HH. Effects of cadmium stress on photosynthetic and characteristics, chlorophyll fluorescence in leaves of flue-cured tobacco[J]. Acta Agric Bor-Sin, 2016, 31:388-393]
23 Krause GH, Winter K. Photoinhibition of photosynthesis in plants growing in natural tropical forest gaps:a chlorophyll fluorescence study[J]. Plant Biol, 2015, 109(6):456-462
24 Rehman AU, Cser K, Sass L, Vass I. Characterization of singlet oxygen production and its involvement in photodamage of acclimation of kidney bean(Phaseolus vulgaris). Photosynthetica, 2015, 53(2):195-200
25 吴强,李红玉,张立新,梁厚果.环境胁迫与植物抗氰呼吸[J].西北植物学报, 2003, 23(1):164-170[Wu Q, Li HY, Zhang LX, Liang HG.The stresses and thecyanide-resistant respiration[J].Acta Bot Bor Occid Sin, 2003, 23(1):164-170]