外源乙烯对镉处理下玉米幼苗生理代谢的影响
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摘要
为探讨外源乙烯缓解玉米(Zea mays)幼苗镉(Cd)毒害的生理机制,通过水培试验研究了Cd处理下,外源乙烯对玉米幼苗相关生理指标与Cd的亚细胞分布的影响,以不做任何处理为空白对照,以Cd处理和(NH4)2SO4处理为试验对照。结果显示,相对Cd处理,乙烯和(NH4)2SO4处理可显著降低Cd胁迫下玉米幼苗H2O2和丙二醛(MDA)含量,使净光合速率分别提升1.23倍和1.22倍;显著降低抗氧化物酶[超氧化物歧化酶(SOD)、过氧化氢酶(CAT)]活性,抗氧化物质[抗坏血酸(AsA)、谷胱甘肽(GSH)]含量则显著上升。另外,相对于Cd处理,乙烯+Cd处理可使玉米幼苗ATP硫酸化酶活性、谷胱甘肽还原酶(GR)活性、半胱氨酸和还原型谷胱甘肽(GSH)含量分别上升54.43%、27.93%、50.77%和49.85%,而对非蛋白硫醇(NPT)和植物螯合素(PCs)含量无显著性影响。在乙烯+Cd处理的基础上添加GSH合成抑制剂BSO(buthionine sulfoximine)可导致玉米叶片GSH含量显著降低, H_2O_2含量上升,光合速率下降。外源乙烯可显著降低Cd胁迫下玉米叶片Cd含量,而显著提升根部细胞壁和液泡中Cd含量。因此,外源乙烯一方面通过提升玉米叶片GSH和AsA含量,增强叶片非酶促抗氧化能力,而非通过抗氧化酶促反应和NPT、PCs的螯合作用;另一方面则通过根细胞壁的固定作用和液泡区室化作用,减少Cd向玉米叶片中的转移,从而缓解Cd毒害。研究结果可为乙烯作为潜在的作物重金属拮抗剂提供理论依据。
There has been increasing heavy metals [especially cadmium(Cd)] pollution in farmlands in China. Studies have identified the crucial role of exogenous ethylene in the reversal of Cd stress in plants such as Arabidopsis thaliana mustard. However, few studies have been done on maize(Zea mays), which is the second largest staple crop in China. To investigate the potential process by which exogenous ethylene alleviates Cd stress in maize, hydroponic experiments were conducted. The experiments included a treatment that served as a blank control and others that were Cd and(NH_4)_2 SO_4 treatments. Changes in physiological indexes of maize seedling leaf along with subcellular distribution of Cd in leaves and roots of the plant were determined under Cd treatment, exogenous ethylene treatment and exogenous sulphur treatment. The results suggested that H_2O_2 and malondialdehyde(MDA) contents of maize seedling leaf decreased under exogenous ethylene and exogenous(NH_4)_2SO_4 treatments, comparing with Cd treatment alone.Also, the rate of net photosynthesis was promoted by 1.23 times and 1.22 times respectively under exogenous ethylene and exogenous(NH4)2 SO4 treatments. The activity of antioxidant enzymes [superoxide diamutase(SOD), catalase(CAT)] significantly decreased, while the contents of antioxidants [ascorbic acid(AsA) and glutathione(GSH)] significantly increased under exogenous ethylene or exogenous(NH_4)_2SO_4 treatments with Cd stress. The results suggested that exogenous ethylene reduced Cd-induced oxidative stress and the degree of lipid peroxidation by enhancing non-enzymatic antioxidant reaction. However, it did not affect enzymatic antioxidant reaction, but then promoted photosynthetic processes. Compared with Cd treatment alone, the activities of ATP sulfurylase and glutathione reductase(GR), and the contents of cysteine and GSH in maize seedlings increased respectively by54.43%, 27.93%, 50.77%, and 49.85% with exogenous ethylene treatment. However, there was no significant change in non-protein thio(NPT) and phytochelatins(PCs) contents. The results showed that ethylene potentiated GSH biosynthesis to resist Cd conditions.To show this that was the case, a GSH biosynthetic inhibitor — buthionine sulfoximine(BSO) — was applied on maize seedlings under Cd and exogenous ethylene conditions. Compared with Cd plus exogenous ethylene treatment, BSO significantly decreased GSH content, increased H_2O_2 content and reduced net photosynthesis rate. Furthermore, Cd content in roots significantly increased while it decreased in leaves after treatment with exogenous ethylene under Cd stress. Further analysis showed that Cd content in cell wall and vacuole of roots was enhanced with exogenous ethylene treatment. Totally, exogenous ethylene reversal of the effect of Cd stress on maize was a complex process involving the promotion of GSH and AsA contents and Cd distribution in roots. On the one hand, exogenous ethylene treatment enhanced non-enzymatic antioxidant capacity by increasing the contents of GSH and AsA, and not by improving the activities of antioxidant enzymes nor chelating NPT and PC in maize leaf. On the other hand, translocation of Cd from maize root to leaf was reduced by enhancing Cd sequestration in cell walls and vacuoles of maize root. The results provided the fundamental information for the application of ethylene in the reversal of heavy metal stress.
There has been increasing heavy metals [especially cadmium(Cd)] pollution in farmlands in China. Studies have identified the crucial role of exogenous ethylene in the reversal of Cd stress in plants such as Arabidopsis thaliana mustard. However, few studies have been done on maize(Zea mays), which is the second largest staple crop in China. To investigate the potential process by which exogenous ethylene alleviates Cd stress in maize, hydroponic experiments were conducted. The experiments included a treatment that served as a blank control and others that were Cd and(NH_4)_2 SO_4 treatments. Changes in physiological indexes of maize seedling leaf along with subcellular distribution of Cd in leaves and roots of the plant were determined under Cd treatment, exogenous ethylene treatment and exogenous sulphur treatment. The results suggested that H_2O_2 and malondialdehyde(MDA) contents of maize seedling leaf decreased under exogenous ethylene and exogenous(NH_4)_2SO_4 treatments, comparing with Cd treatment alone.Also, the rate of net photosynthesis was promoted by 1.23 times and 1.22 times respectively under exogenous ethylene and exogenous(NH4)2 SO4 treatments. The activity of antioxidant enzymes [superoxide diamutase(SOD), catalase(CAT)] significantly decreased, while the contents of antioxidants [ascorbic acid(AsA) and glutathione(GSH)] significantly increased under exogenous ethylene or exogenous(NH_4)_2SO_4 treatments with Cd stress. The results suggested that exogenous ethylene reduced Cd-induced oxidative stress and the degree of lipid peroxidation by enhancing non-enzymatic antioxidant reaction. However, it did not affect enzymatic antioxidant reaction, but then promoted photosynthetic processes. Compared with Cd treatment alone, the activities of ATP sulfurylase and glutathione reductase(GR), and the contents of cysteine and GSH in maize seedlings increased respectively by54.43%, 27.93%, 50.77%, and 49.85% with exogenous ethylene treatment. However, there was no significant change in non-protein thio(NPT) and phytochelatins(PCs) contents. The results showed that ethylene potentiated GSH biosynthesis to resist Cd conditions.To show this that was the case, a GSH biosynthetic inhibitor — buthionine sulfoximine(BSO) — was applied on maize seedlings under Cd and exogenous ethylene conditions. Compared with Cd plus exogenous ethylene treatment, BSO significantly decreased GSH content, increased H_2O_2 content and reduced net photosynthesis rate. Furthermore, Cd content in roots significantly increased while it decreased in leaves after treatment with exogenous ethylene under Cd stress. Further analysis showed that Cd content in cell wall and vacuole of roots was enhanced with exogenous ethylene treatment. Totally, exogenous ethylene reversal of the effect of Cd stress on maize was a complex process involving the promotion of GSH and AsA contents and Cd distribution in roots. On the one hand, exogenous ethylene treatment enhanced non-enzymatic antioxidant capacity by increasing the contents of GSH and AsA, and not by improving the activities of antioxidant enzymes nor chelating NPT and PC in maize leaf. On the other hand, translocation of Cd from maize root to leaf was reduced by enhancing Cd sequestration in cell walls and vacuoles of maize root. The results provided the fundamental information for the application of ethylene in the reversal of heavy metal stress.
引文
[1]李婧,周艳文,陈森,等.我国土壤镉污染现状、危害及其治理方法综述[J].安徽农学通报,2015,21(24):104-107LI J,ZHOU Y W,CHEN S,et al.Actualities,damage and management of soil cadmium pollution in China[J].Anhui Agricultural Science Bulletin,2015,21(24):104-107
[2]KOVá?IK J,BABULA P,KLEJDUS B,et al.Comparison of oxidative stress in four Tillandsia species exposed to cadmium[J].Plant Physiology and Biochemistry,2014,80:33-40
[3]CHOPPALA G,SAIFULLAH,BOLAN N,et al.Cellular mechanisms in higher plants governing tolerance to cadmium toxicity[J].Critical Reviews in Plant Sciences,2014,33(5):374-391
[4]RIZWAN M,ALI S,ADREES M,et al.A critical review on effects,tolerance mechanisms and management of cadmium in vegetables[J].Chemosphere,2017,182:90-105
[5]CHANEY R L.How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers[J].Current Pollution Reports,2015,1(1):13-22
[6]HUGUET S,BERT V,LABOUDIGUE A,et al.Cd speciation and localization in the hyperaccumulator Arabidopsis halleri[J].Environmental and Experimental Botany,2012,82:54-65
[7]VERBRUGGEN N,HERMANS C,SCHAT H.Molecular mechanisms of metal hyperaccumulation in plants[J].New Phytologist,2009,181(4):759-776
[8]薛洪宝,常华兰,陶兆林,等.玉米发芽过程中Cd和硫醇化合物相互作用的研究[J].农业环境科学学报,2011,30(5):824-829XUE H B,CHANG H L,TAO Z L,et al.The interaction between Cd and thiol compounds during the maize seed germination[J].Journal of Agro-Environment Science,2011,30(5):824-829
[9]COBBETT C S.Phytochelatins and their roles in heavy metal detoxification[J].Plant Physiology,2000,123(3):825-832
[10]WANG F F,CUI X K,SUN Y,et al.Ethylene signaling and regulation in plant growth and stress responses[J].Plant Cell Reports,2013,32(7):1099-1109
[11]于延文.乙烯和赤霉素调控植物耐逆性的分子基础[D].保定:河北农业大学,2016YU Y W.Molecular mechanism of ethylene and gibberelin in regulating stress tolerance[D].Baoding:Hebei Agricultural University,2016
[12]VAN LOON L C,GERAATS B P J,LINTHORST H J M.Ethylene as a modulator of disease resistance in plants[J].Trends in Plant Science,2006,11(4):184-191
[13]ACHARD P,CHENG H,DE GRAUWE L,et al.Integration of plant responses to environmentally activated phytohormonal signals[J].Science,2006,311(5757):91-94
[14]KHAN N A,ASGHER M,PER T S,et al.Ethylene potentiates sulfur-mediated reversal of cadmium inhibited photosynthetic responses in mustard[J].Frontiers in Plant Science,2016,7:1628
[15]刘艳菊.外源镉及乙烯对拟南芥幼苗生理代谢的影响研究[D].哈尔滨:东北林业大学,2013LIU Y J.Studies on physiological metabolism of arabidopsis under exogenous cadmium and ethylene[D].Harbin:Northeast Forestry University,2013
[16]陈丹丹.乙烯调节镉胁迫下拟南芥根构型的研究[D].哈尔滨:东北林业大学,2014CHEN D D.Studies on ethylene regulate root configuration of arabidopsis under cadmium stress[D].Harbin:Northeast Forestry University,2014
[17]祁迎春,王建,陆斌,等.榆林市区周边土壤重金属污染特征与评价[J].陕西农业科学,2017,63(6):50-53QI Y C,WANG J,LU B,et al.The characteristics and evaluation of heavy metal contamination for soils at the suburb of Yulin City[J].Shaanxi Journal of Agricultural Sciences,2017,63(6):50-53
[18]王玉萍,常宏,李成,等.Ca2+对镉胁迫下玉米幼苗生长、光合特征和PSⅡ功能的影响[J].草业学报,2016,25(5):40-48WANG Y P,CHANG H,LI C,et al.Effects of exogenous Ca2+on growth,photosynthetic characteristics and photosystemⅡfunction of maize seedlings under cadmium stress[J].Acta Prataculturae Sinica,2016,25(5):40-48
[19]OKUDA T,MATSUDA Y,YAMANAKA A,et al.Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment[J].Plant Physiology,1991,97(3):1265-1267
[20]张志良,瞿伟菁.植物生理学实验指导[M].第3版.北京:高等教育出版社,2003ZHANG Z L,QU W J.The Experimental Guide for Plant Physiology[M].3rd ed.Beijing:High Education Press,2003
[21]PER T S,MASOOD A,KHAN N A.Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard(Brassica juncea L.)[J].Nitric Oxide,2017,68:111-124
[22]ZHOU W,ZHAO D,LIN X.Effects of waterlogging on nitrogen accumulation and alleviation of waterlogging damage by application of nitrogen fertilizer and mixtalol in winter rape(Brassica napus L.)[J].Journal of Plant Growth Regulation,1997,16(1):47-53
[23]AEBI H.Catalase in vitro[J].Methods in Enzymology,1984,105:121-126
[24]FOYER C H,HALLIWELL B.The presence of glutathione and glutathione reductase in chloroplasts:A proposed role in ascorbic acid metabolism[J].Planta,1976,133(1):21-25
[25]ANDERSON M E.Determination of glutathione and glutathione disulfide in biological samples[J].Methods in Enzymology,1985,113:548-555
[26]GAITONDE M K.A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids[J].Biochemical Journal,1967,104(2):627-633
[27]DEVI S R,PRASAD M N V.Copper toxicity in Ceratophyllum demersum L.(coontail),a free floating macrophyte:Response of antioxidant enzymes and antioxidants[J].Plant Science,1998,138(2):157-165
[28]潘瑶,尹洁,高子平,等.硫对水稻幼苗镉积累特性及亚细胞分布特征的影响[J].农业资源与环境学报,2015,32(3):275-281PAN Y,YIN J,GAO Z P,et al.Effects of sulfur on the accumulation and subcellular distribution of cadmium in rice seedlings[J].Journal of Agricultural Resources and Environment,2015,32(3):275-281
[29]张雯.硫硒交互对水稻幼苗镉累积和毒害的影响机制研究[D].上海:华东理工大学,2014ZHANG W.Influence mechanism of sulfur and selenium interaction on cadmium accumulation and toxicity in rice seedling[D].Shanghai:East China University of Science and Technology,2014
[30]APEL K,HIRT H.Reactive oxygen species:Metabolism,oxidative stress,and signal transduction[J].Annual Review of Plant Biology,2004,55:373-399
[31]ABOZEID A,YING Z J,LIN Y C,et al.Ethylene improves root system development under cadmium stress by modulating superoxide anion concentration in Arabidopsis thaliana[J].Frontiers in Plant Science,2017,8:253
[32]MASOOD A,KHAN M I R,FATMA M,et al.Involvement of ethylene in gibberellic acid-induced sulfur assimilation,photosynthetic responses,and alleviation of cadmium stress in mustard[J].Plant Physiology and Biochemistry,2016,104:1-10
[33]DONG Y J,CHEN W F,XU L L,et al.Nitric oxide can induce tolerance to oxidative stress of peanut seedlings under cadmium toxicity[J].Plant Growth Regulation,2016,79(1):19-28
[34]MENDOZA-CóZATL D G,MORENO-SáNCHEZ R.Control of glutathione and phytochelatin synthesis under cadmium stress.Pathway modeling for plants[J].Journal of Theoretical Biology,2006,238(4):919-936
[35]LIANG T,DING H,WANG G D,et al.Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulfur assimilation and glutathione metabolism in Brassica chinensis L.[J].Ecotoxicology and Environmental Safety,2016,124:129-137
[36]LUO L L,KANG J Q,PANG H X,et al.Sulfur protects pakchoi(Brassica chinensis L.)seedlings against cadmium stress by regulating ascorbate-glutathione metabolism[J].International Journal of Molecular Sciences,2017,18(8):1628
[37]ZHAO H,JIN Q J,WANG Y J,et al.Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia[J].Plant Growth Regulation,2016,78(2):243-251
[38]WóJCIK M,DRESLER S,PLAK A,et al.Naturally evolved enhanced Cd tolerance of Dianthus carthusianorum L.is not related to accumulation of thiol peptides and organic acids[J].Environmental Science and Pollution Research,2015,22(10):7906-7917
[39]EBBS S,LAU I,AHNER B,et al.Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens(J.&C.Presl)[J].Planta,2002,214(4):635-640
[2]KOVá?IK J,BABULA P,KLEJDUS B,et al.Comparison of oxidative stress in four Tillandsia species exposed to cadmium[J].Plant Physiology and Biochemistry,2014,80:33-40
[3]CHOPPALA G,SAIFULLAH,BOLAN N,et al.Cellular mechanisms in higher plants governing tolerance to cadmium toxicity[J].Critical Reviews in Plant Sciences,2014,33(5):374-391
[4]RIZWAN M,ALI S,ADREES M,et al.A critical review on effects,tolerance mechanisms and management of cadmium in vegetables[J].Chemosphere,2017,182:90-105
[5]CHANEY R L.How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers[J].Current Pollution Reports,2015,1(1):13-22
[6]HUGUET S,BERT V,LABOUDIGUE A,et al.Cd speciation and localization in the hyperaccumulator Arabidopsis halleri[J].Environmental and Experimental Botany,2012,82:54-65
[7]VERBRUGGEN N,HERMANS C,SCHAT H.Molecular mechanisms of metal hyperaccumulation in plants[J].New Phytologist,2009,181(4):759-776
[8]薛洪宝,常华兰,陶兆林,等.玉米发芽过程中Cd和硫醇化合物相互作用的研究[J].农业环境科学学报,2011,30(5):824-829XUE H B,CHANG H L,TAO Z L,et al.The interaction between Cd and thiol compounds during the maize seed germination[J].Journal of Agro-Environment Science,2011,30(5):824-829
[9]COBBETT C S.Phytochelatins and their roles in heavy metal detoxification[J].Plant Physiology,2000,123(3):825-832
[10]WANG F F,CUI X K,SUN Y,et al.Ethylene signaling and regulation in plant growth and stress responses[J].Plant Cell Reports,2013,32(7):1099-1109
[11]于延文.乙烯和赤霉素调控植物耐逆性的分子基础[D].保定:河北农业大学,2016YU Y W.Molecular mechanism of ethylene and gibberelin in regulating stress tolerance[D].Baoding:Hebei Agricultural University,2016
[12]VAN LOON L C,GERAATS B P J,LINTHORST H J M.Ethylene as a modulator of disease resistance in plants[J].Trends in Plant Science,2006,11(4):184-191
[13]ACHARD P,CHENG H,DE GRAUWE L,et al.Integration of plant responses to environmentally activated phytohormonal signals[J].Science,2006,311(5757):91-94
[14]KHAN N A,ASGHER M,PER T S,et al.Ethylene potentiates sulfur-mediated reversal of cadmium inhibited photosynthetic responses in mustard[J].Frontiers in Plant Science,2016,7:1628
[15]刘艳菊.外源镉及乙烯对拟南芥幼苗生理代谢的影响研究[D].哈尔滨:东北林业大学,2013LIU Y J.Studies on physiological metabolism of arabidopsis under exogenous cadmium and ethylene[D].Harbin:Northeast Forestry University,2013
[16]陈丹丹.乙烯调节镉胁迫下拟南芥根构型的研究[D].哈尔滨:东北林业大学,2014CHEN D D.Studies on ethylene regulate root configuration of arabidopsis under cadmium stress[D].Harbin:Northeast Forestry University,2014
[17]祁迎春,王建,陆斌,等.榆林市区周边土壤重金属污染特征与评价[J].陕西农业科学,2017,63(6):50-53QI Y C,WANG J,LU B,et al.The characteristics and evaluation of heavy metal contamination for soils at the suburb of Yulin City[J].Shaanxi Journal of Agricultural Sciences,2017,63(6):50-53
[18]王玉萍,常宏,李成,等.Ca2+对镉胁迫下玉米幼苗生长、光合特征和PSⅡ功能的影响[J].草业学报,2016,25(5):40-48WANG Y P,CHANG H,LI C,et al.Effects of exogenous Ca2+on growth,photosynthetic characteristics and photosystemⅡfunction of maize seedlings under cadmium stress[J].Acta Prataculturae Sinica,2016,25(5):40-48
[19]OKUDA T,MATSUDA Y,YAMANAKA A,et al.Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment[J].Plant Physiology,1991,97(3):1265-1267
[20]张志良,瞿伟菁.植物生理学实验指导[M].第3版.北京:高等教育出版社,2003ZHANG Z L,QU W J.The Experimental Guide for Plant Physiology[M].3rd ed.Beijing:High Education Press,2003
[21]PER T S,MASOOD A,KHAN N A.Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard(Brassica juncea L.)[J].Nitric Oxide,2017,68:111-124
[22]ZHOU W,ZHAO D,LIN X.Effects of waterlogging on nitrogen accumulation and alleviation of waterlogging damage by application of nitrogen fertilizer and mixtalol in winter rape(Brassica napus L.)[J].Journal of Plant Growth Regulation,1997,16(1):47-53
[23]AEBI H.Catalase in vitro[J].Methods in Enzymology,1984,105:121-126
[24]FOYER C H,HALLIWELL B.The presence of glutathione and glutathione reductase in chloroplasts:A proposed role in ascorbic acid metabolism[J].Planta,1976,133(1):21-25
[25]ANDERSON M E.Determination of glutathione and glutathione disulfide in biological samples[J].Methods in Enzymology,1985,113:548-555
[26]GAITONDE M K.A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids[J].Biochemical Journal,1967,104(2):627-633
[27]DEVI S R,PRASAD M N V.Copper toxicity in Ceratophyllum demersum L.(coontail),a free floating macrophyte:Response of antioxidant enzymes and antioxidants[J].Plant Science,1998,138(2):157-165
[28]潘瑶,尹洁,高子平,等.硫对水稻幼苗镉积累特性及亚细胞分布特征的影响[J].农业资源与环境学报,2015,32(3):275-281PAN Y,YIN J,GAO Z P,et al.Effects of sulfur on the accumulation and subcellular distribution of cadmium in rice seedlings[J].Journal of Agricultural Resources and Environment,2015,32(3):275-281
[29]张雯.硫硒交互对水稻幼苗镉累积和毒害的影响机制研究[D].上海:华东理工大学,2014ZHANG W.Influence mechanism of sulfur and selenium interaction on cadmium accumulation and toxicity in rice seedling[D].Shanghai:East China University of Science and Technology,2014
[30]APEL K,HIRT H.Reactive oxygen species:Metabolism,oxidative stress,and signal transduction[J].Annual Review of Plant Biology,2004,55:373-399
[31]ABOZEID A,YING Z J,LIN Y C,et al.Ethylene improves root system development under cadmium stress by modulating superoxide anion concentration in Arabidopsis thaliana[J].Frontiers in Plant Science,2017,8:253
[32]MASOOD A,KHAN M I R,FATMA M,et al.Involvement of ethylene in gibberellic acid-induced sulfur assimilation,photosynthetic responses,and alleviation of cadmium stress in mustard[J].Plant Physiology and Biochemistry,2016,104:1-10
[33]DONG Y J,CHEN W F,XU L L,et al.Nitric oxide can induce tolerance to oxidative stress of peanut seedlings under cadmium toxicity[J].Plant Growth Regulation,2016,79(1):19-28
[34]MENDOZA-CóZATL D G,MORENO-SáNCHEZ R.Control of glutathione and phytochelatin synthesis under cadmium stress.Pathway modeling for plants[J].Journal of Theoretical Biology,2006,238(4):919-936
[35]LIANG T,DING H,WANG G D,et al.Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulfur assimilation and glutathione metabolism in Brassica chinensis L.[J].Ecotoxicology and Environmental Safety,2016,124:129-137
[36]LUO L L,KANG J Q,PANG H X,et al.Sulfur protects pakchoi(Brassica chinensis L.)seedlings against cadmium stress by regulating ascorbate-glutathione metabolism[J].International Journal of Molecular Sciences,2017,18(8):1628
[37]ZHAO H,JIN Q J,WANG Y J,et al.Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia[J].Plant Growth Regulation,2016,78(2):243-251
[38]WóJCIK M,DRESLER S,PLAK A,et al.Naturally evolved enhanced Cd tolerance of Dianthus carthusianorum L.is not related to accumulation of thiol peptides and organic acids[J].Environmental Science and Pollution Research,2015,22(10):7906-7917
[39]EBBS S,LAU I,AHNER B,et al.Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens(J.&C.Presl)[J].Planta,2002,214(4):635-640