NO对Cd~(2+)胁迫下绿豆幼苗DNA及光合作用的影响
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摘要
以绿豆幼苗为材料,研究了外源一氧化氮(NO)处理对Cd~(2+)胁迫3天和8天时幼苗叶片和根系DNA含量、DNA链间交联程度以及叶片光合参数的影响。结果表明:单独Cd~(2+)胁迫导致叶片和根系DNA含量降低,DNA链间交联程度增加,叶片净光合速率、气孔导度和胞间隙CO2浓度降低,气孔限制值升高;与单独Cd~(2+)胁迫相比,NO和Cd~(2+)复合处理提高了叶片和根系DNA含量,降低了DNA链间交联程度,同时使叶片净光合速率和气孔导度升高,而使胞间隙CO2浓度和气孔限制值降低。结果说明,NO能缓解Cd~(2+)胁迫对绿豆幼苗DNA结构及其代谢的影响;Cd~(2+)胁迫抑制绿豆幼苗光合作用的主要原因是气孔因素,而NO主要通过提高幼苗叶片非气孔因素缓解了Cd~(2+)胁迫对幼苗光合作用的抑制。
Background, aim, and scope With the acceleration of the industrialization process, heavy metal pollution has become one of the hot issues in the world. Cd~(2+) is a more common heavy metal pollutant, so the effect of Cd~(2+) stress on plants has been widely concerned. Previous studies have shown that Cd~(2+) stress has toxic effects on many aspects of plant growth and development, including plant DNA and photosynthesis. So, it is important to explore the safe and effective methods to alleviate the toxic effects of Cd~(2+) pollution on plants, but the researches on these topic are still less. Nitric oxide(NO) acting as a new signaling molecule plays an important role in plant growth and development, defence responses and stress resistance. Previous studies have shown that NO can alleviate the toxic effects of some stresses on plants, such as drought stress, salt stress, hot stress and low temperature stress. However, whether and how NO alleviates the toxic effects of heavy metal stresses on plants are still less known. The aim of this paper is to explore whether and how NO alleviates the toxic effects of Cd~(2+) stress on plant DNA and photosynthesis. Materials and methods In this study, seedlings of mung bean(Phaseolus raditus L. cv. Qindou-20) were used as plant materials, grown in plant growth chambers under a 14 h photoperiod(300 — 3500 μmol · m-2 · s-1), at a day/night temperature cycle of(25 ± 2)℃/(20 ± 2)℃ and a relative humidity of 75% and incubated in 1/2 Hoagland solution. After 33 h of seedling growth, all the seedlings were divided into four groups and transferred to 1/2 Hoagland solution alone(CK), 1/2 Hoagland solution containing 50 μmol · L-1 NO donor sodium nitroprusside(SNP), 1/2 Hoagland solution containing 5 μmol · L-1 Cd Cl2(Cd~(2+)) or 1/2 Hoagland solution containing 50 μmol · L-1 SNP and 5 μmol · L-1 Cd Cl2(SNP + Cd~(2+)), respectively. When seedlings were treated for 3 d and 8 d, the net photosynthetic rate(Pn), stomatal conductance(Gs), and intercellular CO2 concentration(Ci) were measured with a portable CIRAS-2 type photosynthesis system(PP Systems) and stomatal limitation(Ls) was calculated with the formula Ls =(Ao-Ai)/Ao×100%, where Ao is the Pn when Ci is equal to the atmospheric CO2 concentration, and Ai is the Pn at the atmospheric CO2 concentration. DNA contents and DNA hyperchromicity were measured with TU-1800 s UV spectrophotometer. Results Compared to CK, Cd~(2+) stress alone reduced DNA content, enhanced the degree of cross-linking between DNA chains in leaves and roots, decreased Pn, Gs and Ci and increased Ls in leaves. Compared to Cd~(2+) stress alone, the combined treatment of exogenous NO and Cd~(2+) increased DNA content and decreased the cross-linking between DNA chains in leaves and roots, while Pn and Gs were increased, and Ci and Ls were decreased in leaves. Discussion In consistent with the results of previous studies, our results in this paper also show that Cd~(2+) stress has the toxic effects on plant DNA and photosynthesis. Furthermore, our results clearly show that exogenous NO can effectively alleviate the toxic effects of Cd~(2+) stress on plant DNA and photosynthesis. In addition, although previous studies have paid much attention on the inhibitory mechanisms of Cd~(2+) stress on photosynthesis, it is still unclear which factor between stomatal and nonstomatal limitations plays more important role during different stages of Cd~(2+) stress-inhibited photosynthesis. Our results in this paper indicate that the stomatal limitation plays a more important role during the early stage of Cd~(2+) stress-induced inhibition of photosynthesis. Combined with the previous results, we suggest that under Cd~(2+) stress, the inhibition of photosynthesis in mung bean leaves is the results of both stomatal and nonstomatal limitations, but the stomatal limitation is dominant during early stage, nonstomatal limitation becomes the dominant one during late stage. Moreover, our results also show that exogenous NO alleviates the inhibitory effects of Cd~(2+) stress on photosynthesis mainly by improving the photosynthetic activity of seedling mesophyll cells. Conclusions(1) Exogenous NO can effectively alleviate the toxic effects of Cd~(2+) stress on DNA and photosynthesis in mung bean seedlings;(2) Stomatal limitation plays a more important role during the early stage of Cd~(2+) stress-inhibited photosynthesis;(3) NO alleviates the inhibitory effects of Cd~(2+) stress on photosynthesis mainly by improving the photosynthetic activity of mesophyll cells. Recommendations and perspectives Although our results show that NO can effectively alleviate the toxic effects of Cd~(2+) stress on DNA and photosynthesis, the detailed mechanisms underlining these processes are still unclear, which should be studied in the future.
Background, aim, and scope With the acceleration of the industrialization process, heavy metal pollution has become one of the hot issues in the world. Cd~(2+) is a more common heavy metal pollutant, so the effect of Cd~(2+) stress on plants has been widely concerned. Previous studies have shown that Cd~(2+) stress has toxic effects on many aspects of plant growth and development, including plant DNA and photosynthesis. So, it is important to explore the safe and effective methods to alleviate the toxic effects of Cd~(2+) pollution on plants, but the researches on these topic are still less. Nitric oxide(NO) acting as a new signaling molecule plays an important role in plant growth and development, defence responses and stress resistance. Previous studies have shown that NO can alleviate the toxic effects of some stresses on plants, such as drought stress, salt stress, hot stress and low temperature stress. However, whether and how NO alleviates the toxic effects of heavy metal stresses on plants are still less known. The aim of this paper is to explore whether and how NO alleviates the toxic effects of Cd~(2+) stress on plant DNA and photosynthesis. Materials and methods In this study, seedlings of mung bean(Phaseolus raditus L. cv. Qindou-20) were used as plant materials, grown in plant growth chambers under a 14 h photoperiod(300 — 3500 μmol · m-2 · s-1), at a day/night temperature cycle of(25 ± 2)℃/(20 ± 2)℃ and a relative humidity of 75% and incubated in 1/2 Hoagland solution. After 33 h of seedling growth, all the seedlings were divided into four groups and transferred to 1/2 Hoagland solution alone(CK), 1/2 Hoagland solution containing 50 μmol · L-1 NO donor sodium nitroprusside(SNP), 1/2 Hoagland solution containing 5 μmol · L-1 Cd Cl2(Cd~(2+)) or 1/2 Hoagland solution containing 50 μmol · L-1 SNP and 5 μmol · L-1 Cd Cl2(SNP + Cd~(2+)), respectively. When seedlings were treated for 3 d and 8 d, the net photosynthetic rate(Pn), stomatal conductance(Gs), and intercellular CO2 concentration(Ci) were measured with a portable CIRAS-2 type photosynthesis system(PP Systems) and stomatal limitation(Ls) was calculated with the formula Ls =(Ao-Ai)/Ao×100%, where Ao is the Pn when Ci is equal to the atmospheric CO2 concentration, and Ai is the Pn at the atmospheric CO2 concentration. DNA contents and DNA hyperchromicity were measured with TU-1800 s UV spectrophotometer. Results Compared to CK, Cd~(2+) stress alone reduced DNA content, enhanced the degree of cross-linking between DNA chains in leaves and roots, decreased Pn, Gs and Ci and increased Ls in leaves. Compared to Cd~(2+) stress alone, the combined treatment of exogenous NO and Cd~(2+) increased DNA content and decreased the cross-linking between DNA chains in leaves and roots, while Pn and Gs were increased, and Ci and Ls were decreased in leaves. Discussion In consistent with the results of previous studies, our results in this paper also show that Cd~(2+) stress has the toxic effects on plant DNA and photosynthesis. Furthermore, our results clearly show that exogenous NO can effectively alleviate the toxic effects of Cd~(2+) stress on plant DNA and photosynthesis. In addition, although previous studies have paid much attention on the inhibitory mechanisms of Cd~(2+) stress on photosynthesis, it is still unclear which factor between stomatal and nonstomatal limitations plays more important role during different stages of Cd~(2+) stress-inhibited photosynthesis. Our results in this paper indicate that the stomatal limitation plays a more important role during the early stage of Cd~(2+) stress-induced inhibition of photosynthesis. Combined with the previous results, we suggest that under Cd~(2+) stress, the inhibition of photosynthesis in mung bean leaves is the results of both stomatal and nonstomatal limitations, but the stomatal limitation is dominant during early stage, nonstomatal limitation becomes the dominant one during late stage. Moreover, our results also show that exogenous NO alleviates the inhibitory effects of Cd~(2+) stress on photosynthesis mainly by improving the photosynthetic activity of seedling mesophyll cells. Conclusions(1) Exogenous NO can effectively alleviate the toxic effects of Cd~(2+) stress on DNA and photosynthesis in mung bean seedlings;(2) Stomatal limitation plays a more important role during the early stage of Cd~(2+) stress-inhibited photosynthesis;(3) NO alleviates the inhibitory effects of Cd~(2+) stress on photosynthesis mainly by improving the photosynthetic activity of mesophyll cells. Recommendations and perspectives Although our results show that NO can effectively alleviate the toxic effects of Cd~(2+) stress on DNA and photosynthesis, the detailed mechanisms underlining these processes are still unclear, which should be studied in the future.
引文
陈国祥,施国新,何兵,等.1999.Hg、Cd对莼菜越冬芽光合膜光化学活性及多肽组分的影响[J].环境科学学报,19(5):521-525.[Chen G X,Shi G X,He B,et al.1999.Effect of mercury and cadmium on photochemical activity and polypeptide compositions of photosynthetic membranes from winter bud of Brasenia schreberi[J].Acta Scientiae Circumstantiae,19(5):521-525.]
陈明,沈文飚,阮海华,等.2004.一氧化氮对盐胁迫下小麦幼苗根生长和氧化损伤的影响[J].植物生理与分子生物学学报,30(5):569-576.[Chen M,Shen W B,Ruan H H,et al.2004.Effects of nitric oxide on root growth and its oxidative damage in wheat seedlings under salt stress[J].Journal of Plant Physiology and Molecular Biology,30(5):569-576.]
陈霞,杨文胜,靳健,等.2001.Cd2+离子诱导的DNA构象变化[J].高等学校化学学报,22(7):1228-1229.[Chen X,Yang W S,Jin J,et al.2001.Cd2+ions induced conformation change of DNA[J].Chemical Journal of Chinese Universities,22(7):1228-1229.]
郭燕梅,王昌全,李冰.2008.重金属镉对植物的毒害研究进展[J].陕西农业科学,54(3):122-125.[Guo Y M,Wang C Q,Li B.2008.Research progress on the toxic effect of heavy metal cadmium on plants[J].Journal of Shaanxi Agriculture Sciences,54(3):122-125.]
李慧,丛郁,王宏伟,等.2010.镉对草莓幼苗根尖氧化系统和基因组DNA损伤的影响[J].园艺学报,37(5):721-730.[Li H,Cong Y,Wang H W,et al.2010.Effects of cadmium stress on oxygen enzyme system and genome DNA polymorphism in the root tips of strawberry plants[J].Acta Horticulturae Sinica,37(5):721-730.]
李蕾蕾.2016.外源NO对干旱条件下玉米幼苗光合特性及抗氧化酶系统的影响[D].郑州:河南农业大学.[Li L L.2016.Effects of exogenous nitric oxide on photosynthetic characteristics and antioxidant enzyme system of maize seedlings under drought stress[D].Zhengzhou:Henan Agricultural University.]
李艳艳,李华,贺军民.2012.外源NO处理对镉胁迫下绿豆幼苗生长的影响[J].陕西农业科学,58(6):55-59+76.[Li Y Y,Li H,He J M.2012.Effects of exogenous NO on growth of mung bean seedlings under cadmium stress[J].Journal of Shaanxi Agriculture Sciences,58(6):55-59+76.]
林单,任妲妮,杨奇贤,等.2010.近10年我国植物对重金属Cd耐性研究文献分析[J].农业图书情报学刊,22(6):13-17.[Lin D,Ren D N,Yang Q X,et al.2010.Analysis of bibliography on cadmium tolerance of plants research in recent ten years in china[J].Journal of Library and Information Sciences in Agriculture,22(6):13-17.]
刘宛,郑乐,李培军,等.2006.镉胁迫对大麦幼苗基因组DNA多态性影响[J].农业环境科学学报,25(1):19-24.[Liu W,Zheng L,Li P J,et al.2006.Effects of cadmium stress on DNA polymorphism of genome in barley seedlings[J].Journal of Agro-Environment Science,25(1):19-24.]
马向丽,魏小红,龙瑞军,等.2005.外源一氧化氮提高一年生黑麦草抗冷性机制[J].生态学报,25(6):1269-1274.[Ma X L,Wei X H,Long R J,et al.2005.Studies on mechanism of enhancing the chilling resistance of annual ryegrass by exogenous nitric oxide[J].Acta Ecologica Snica,25(6):1269-1274.]
马引利,佘小平.2006.铝、镉对小麦幼苗生长的影响及其DNA损伤效应研究[J].西北植物学报,26(4):729-735.[Ma Y L,She X P.2006.Effects and DNA damages of Al3+and Cd2+in wheat seedlings[J].Acta Botanica BorealiOccidentalia Sinica,26(4):729-735.]
牟雪姣,张远兵.2015.NO调节植物低温胁迫抗性机制研究进展[J].长江大学学报(自科版),12(21):34-38+46.[Mu X J,Zhang Y B.2015.Research advances on mechanism of NO regulating resistance to low temperature[J].Journal of Yangtze University(Natural Science Edition),12(21):34-38+46.]
孙德智,杨恒山,彭靖,等.2014.外源SA和NO对Na Cl胁迫下番茄幼苗生长、光合及离子分布的影响[J].生态学报,34(13):3519-3528.[Sun D Z,Yang H S,Peng J,et al.2014.Effects of exogenous salicylic acid and nitric oxide on growth,photosynthesis,and ion distribution in tomato seedlings under Na Cl stress[J].Acta Ecologica Sinica,34(13):3519-3528.]
王松,莘冰茹,周艳,等.2016.外源NO对Na Cl胁迫下番茄幼苗生长及光合特性的影响[J].石河子大学学报(自然科学版),34(3):321-327.[Wang S,Shen B R,Zhou Y,et al.2016.Effect of exogenous nitric oxide on growth and photosynthetic characteristics in tomato seedling under Na Cl stress[J].Journal of Shihezi University(Natural Science),34(3):321-327.]
许大全.1997.光合作用气孔限制分析中的一些问题[J].植物生理学通讯,33(4):241-244.[Xu D Q.1997.Some problem in stomatal limitation analysis of photosynthesis[J].Plant Physiology Communications,33(4):241-244.]
张芬琴,张红晓,沈振国.2012.Cd胁迫下不同耐性豆科植物根内活性氧产生与基因组DNA多态性变化[J].生态学杂志,31(9):2330-2336.[Zhang F Q,Zhang H X,Shen Z G.2012.Reactive oxygen production and genome DNA polymorphism change in root tip tissues of two leguminous species with different tolerance under Cd2+stress[J].Chinese Journal of Ecology,31(9):2330-2336.]
Akio U,Andre T J,Takashi H,et al.2002.Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice[J].Plant Science,163:515-523.
Atienzar F A,Venier P,Jha A N.2002.Evaluation of the random amplified polymorphic DNA(RAPD)assay for the detection of DNA damage and mutations[J].Mutation Research,521:151-163.
Fancy N N,Bahlmann A,Loake G J.2017.Nitric oxide function in plant abiotic stress[J].Plant,Cell and Environment,40:462-472.
Farquhar G D,Sharkey T D.1982.Stomatal conductance and photosynthesis[J].Annual Review of Plant Physiology,33:317-345.
Ghoshroy S,Nadakavukaren M J.1990.Infl uence of cadmium on the ultrastructure of developing chloroplasts in soybean and corn[J].Environmental and Experimental Botany,30:187-192.
Koch C J,Giandomenico A R.1994.The alkaline elution technique for measuring DNA single strand breaks:increased reliability and sensitivity[J].Analytical Biochemistry,220(1):58-65.
Malik D,Sheoran I S,Singh R.1992.Carbon metabolism in leaves of cadmium treated wheat seedlings[J].Plant Physiology and Biochemistry,30:223-229.
Padmaja K,Parsad D D K,Parsad A R K.1990.Inhibition of chlorophyll synthesis in Phaseolus vulgaris L.seedlings by cadmium acetate[J].Photosynthetica,24:399-404.
Sheoran I S,Singal H R,Singh R.1990.Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeon pea(Cajanus cajan L.)[J].Photosynthesis Research,23:345-351.
Tuteja N,Singh M B,Misra M K,et al.2001.Molecular mechanisms of DNA damage and repair:Progress in plants[J].Critical Reviews in Biochemistry and Molecular Biology,36(4):337-397.
Weigel H J.1985.Inhibition of photosynthetic reactions of isolated intact chloroplast by cadmium[J].Journal of Plant Physiology,119:179-189.
陈明,沈文飚,阮海华,等.2004.一氧化氮对盐胁迫下小麦幼苗根生长和氧化损伤的影响[J].植物生理与分子生物学学报,30(5):569-576.[Chen M,Shen W B,Ruan H H,et al.2004.Effects of nitric oxide on root growth and its oxidative damage in wheat seedlings under salt stress[J].Journal of Plant Physiology and Molecular Biology,30(5):569-576.]
陈霞,杨文胜,靳健,等.2001.Cd2+离子诱导的DNA构象变化[J].高等学校化学学报,22(7):1228-1229.[Chen X,Yang W S,Jin J,et al.2001.Cd2+ions induced conformation change of DNA[J].Chemical Journal of Chinese Universities,22(7):1228-1229.]
郭燕梅,王昌全,李冰.2008.重金属镉对植物的毒害研究进展[J].陕西农业科学,54(3):122-125.[Guo Y M,Wang C Q,Li B.2008.Research progress on the toxic effect of heavy metal cadmium on plants[J].Journal of Shaanxi Agriculture Sciences,54(3):122-125.]
李慧,丛郁,王宏伟,等.2010.镉对草莓幼苗根尖氧化系统和基因组DNA损伤的影响[J].园艺学报,37(5):721-730.[Li H,Cong Y,Wang H W,et al.2010.Effects of cadmium stress on oxygen enzyme system and genome DNA polymorphism in the root tips of strawberry plants[J].Acta Horticulturae Sinica,37(5):721-730.]
李蕾蕾.2016.外源NO对干旱条件下玉米幼苗光合特性及抗氧化酶系统的影响[D].郑州:河南农业大学.[Li L L.2016.Effects of exogenous nitric oxide on photosynthetic characteristics and antioxidant enzyme system of maize seedlings under drought stress[D].Zhengzhou:Henan Agricultural University.]
李艳艳,李华,贺军民.2012.外源NO处理对镉胁迫下绿豆幼苗生长的影响[J].陕西农业科学,58(6):55-59+76.[Li Y Y,Li H,He J M.2012.Effects of exogenous NO on growth of mung bean seedlings under cadmium stress[J].Journal of Shaanxi Agriculture Sciences,58(6):55-59+76.]
林单,任妲妮,杨奇贤,等.2010.近10年我国植物对重金属Cd耐性研究文献分析[J].农业图书情报学刊,22(6):13-17.[Lin D,Ren D N,Yang Q X,et al.2010.Analysis of bibliography on cadmium tolerance of plants research in recent ten years in china[J].Journal of Library and Information Sciences in Agriculture,22(6):13-17.]
刘宛,郑乐,李培军,等.2006.镉胁迫对大麦幼苗基因组DNA多态性影响[J].农业环境科学学报,25(1):19-24.[Liu W,Zheng L,Li P J,et al.2006.Effects of cadmium stress on DNA polymorphism of genome in barley seedlings[J].Journal of Agro-Environment Science,25(1):19-24.]
马向丽,魏小红,龙瑞军,等.2005.外源一氧化氮提高一年生黑麦草抗冷性机制[J].生态学报,25(6):1269-1274.[Ma X L,Wei X H,Long R J,et al.2005.Studies on mechanism of enhancing the chilling resistance of annual ryegrass by exogenous nitric oxide[J].Acta Ecologica Snica,25(6):1269-1274.]
马引利,佘小平.2006.铝、镉对小麦幼苗生长的影响及其DNA损伤效应研究[J].西北植物学报,26(4):729-735.[Ma Y L,She X P.2006.Effects and DNA damages of Al3+and Cd2+in wheat seedlings[J].Acta Botanica BorealiOccidentalia Sinica,26(4):729-735.]
牟雪姣,张远兵.2015.NO调节植物低温胁迫抗性机制研究进展[J].长江大学学报(自科版),12(21):34-38+46.[Mu X J,Zhang Y B.2015.Research advances on mechanism of NO regulating resistance to low temperature[J].Journal of Yangtze University(Natural Science Edition),12(21):34-38+46.]
孙德智,杨恒山,彭靖,等.2014.外源SA和NO对Na Cl胁迫下番茄幼苗生长、光合及离子分布的影响[J].生态学报,34(13):3519-3528.[Sun D Z,Yang H S,Peng J,et al.2014.Effects of exogenous salicylic acid and nitric oxide on growth,photosynthesis,and ion distribution in tomato seedlings under Na Cl stress[J].Acta Ecologica Sinica,34(13):3519-3528.]
王松,莘冰茹,周艳,等.2016.外源NO对Na Cl胁迫下番茄幼苗生长及光合特性的影响[J].石河子大学学报(自然科学版),34(3):321-327.[Wang S,Shen B R,Zhou Y,et al.2016.Effect of exogenous nitric oxide on growth and photosynthetic characteristics in tomato seedling under Na Cl stress[J].Journal of Shihezi University(Natural Science),34(3):321-327.]
许大全.1997.光合作用气孔限制分析中的一些问题[J].植物生理学通讯,33(4):241-244.[Xu D Q.1997.Some problem in stomatal limitation analysis of photosynthesis[J].Plant Physiology Communications,33(4):241-244.]
张芬琴,张红晓,沈振国.2012.Cd胁迫下不同耐性豆科植物根内活性氧产生与基因组DNA多态性变化[J].生态学杂志,31(9):2330-2336.[Zhang F Q,Zhang H X,Shen Z G.2012.Reactive oxygen production and genome DNA polymorphism change in root tip tissues of two leguminous species with different tolerance under Cd2+stress[J].Chinese Journal of Ecology,31(9):2330-2336.]
Akio U,Andre T J,Takashi H,et al.2002.Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice[J].Plant Science,163:515-523.
Atienzar F A,Venier P,Jha A N.2002.Evaluation of the random amplified polymorphic DNA(RAPD)assay for the detection of DNA damage and mutations[J].Mutation Research,521:151-163.
Fancy N N,Bahlmann A,Loake G J.2017.Nitric oxide function in plant abiotic stress[J].Plant,Cell and Environment,40:462-472.
Farquhar G D,Sharkey T D.1982.Stomatal conductance and photosynthesis[J].Annual Review of Plant Physiology,33:317-345.
Ghoshroy S,Nadakavukaren M J.1990.Infl uence of cadmium on the ultrastructure of developing chloroplasts in soybean and corn[J].Environmental and Experimental Botany,30:187-192.
Koch C J,Giandomenico A R.1994.The alkaline elution technique for measuring DNA single strand breaks:increased reliability and sensitivity[J].Analytical Biochemistry,220(1):58-65.
Malik D,Sheoran I S,Singh R.1992.Carbon metabolism in leaves of cadmium treated wheat seedlings[J].Plant Physiology and Biochemistry,30:223-229.
Padmaja K,Parsad D D K,Parsad A R K.1990.Inhibition of chlorophyll synthesis in Phaseolus vulgaris L.seedlings by cadmium acetate[J].Photosynthetica,24:399-404.
Sheoran I S,Singal H R,Singh R.1990.Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeon pea(Cajanus cajan L.)[J].Photosynthesis Research,23:345-351.
Tuteja N,Singh M B,Misra M K,et al.2001.Molecular mechanisms of DNA damage and repair:Progress in plants[J].Critical Reviews in Biochemistry and Molecular Biology,36(4):337-397.
Weigel H J.1985.Inhibition of photosynthetic reactions of isolated intact chloroplast by cadmium[J].Journal of Plant Physiology,119:179-189.