叶面喷施二巯基丁二酸对晚稻籽粒镉及矿质元素含量的影响
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摘要
通过考察在水稻开花期叶面喷施一次重金属螯合剂2,3-二巯基丁二酸(DMSA)调控Cd经水稻韧皮部向籽粒中转运,评估将DMSA作为降Cd叶面调理剂的可行性。田间试验过程中,以DMSA为研究对象,采用小区试验法研究了DMSA对Cd及部分矿质元素在水稻不同器官中分布的影响,探讨了DMSA阻控Cd向水稻籽粒迁移转运的机制。结果表明:在晚稻开花期叶面喷施一次DMSA,可使晚稻籽粒中Cd含量降低15.84%～46.09%,穗轴中Cd含量降低10.03%～41.41%,穗颈中Cd含量降低9.13%～28.46%,顶端第一节中Cd含量降低18.30%～38.32%,对其他器官中Cd含量无显著影响。水稻籽粒Cd含量与DMSA喷施浓度在一定范围内呈现出明显的剂量效应关系,但是当喷施浓度超过4 mmol·L-1时籽粒中Cd含量则不再持续降低。喷施DMSA降低了籽粒中Mn含量,但是对其他矿质元素如K、Mg、Ca、Fe、Zn的含量则无显著影响。喷施DMSA显著降低了水稻成熟期旗叶Cd向顶端第一节的转移系数,同时Cd由穗颈向穗轴中的转移系数也表现出降低趋势。据以上结果推测,在水稻开花期叶面喷施DMSA,主要是通过与水稻叶片等组织中的Cd2+形成螯合物来降低Cd向籽粒中的转运。喷施DMSA同时降低晚稻籽粒中Mn含量,是否表明影响了Cd、Mn公用转运基因Nramp5的表达仍有待进一步研究。
Cd pollution in farmland soils has become one of the most important agricultural environmental problems in China. In this study,the feasibility of 2,3-dimercaptosuccinic acid(DMSA)as a foliar modulator for the reduction of rice grain Cd content was evaluated. After spraying DMSA on rice leaves during flowering, we monitored the transport of Cd from phloem to grain. Moreover, we analyzed the effects of DMSA on the distribution of Cd and some other mineral elements in different parts of the rice, and discussed the mechanism through which DMSA could prevent the migration of Cd to the rice grains. The results showed that the application of DMSA on the leaf surface of late rice reduced the rice grain Cd content by 15.84%～46.09%; additionally, the Cd content in the rachis, the first internode, and the first node decreased by 10.03%～41.41%, 9.13%～28.46%, and 18.30%～38.32%, respectively. No significant difference in Cd content was noted in the other organs of the plant. The rice grain Cd content and the concentration of sprayed DMSA showed an obvious dose-effect relationship within a certain range; however, once the spraying concentration exceeded 4 mmol·L-1, the rice grain Cd content did not decrease continuously anymore. The results of this study can be used to support agricultural production. We further noticed that the foliar application of DMSA reduced the rice grain Mn content, but did not have significant effects on the content of other mineral elements(e.g. K, Mg, Ca, Fe,and Zn). After the application of DMSA, the transfer coefficient of Cd from the flag leaf to the first node of the plant was significantly reduced. The transfer coefficient of Cd from the first internode of the plants to the grains also showed a decreasing trend, but the reduction was not significant. According to the above results, the application of DMSA on rice leaves during flowering can reduce the transport of Cd to the grains, mainly through the chelation of Cd2+in the leaves and other tissues of the plant. The Mn content reduction in late rice grains,following the application of DMSA, might indicate that this acid affected the expression of gene Nramp5(a transporter of Cd and Mn); nevertheless, this hypothesis needs to be confirmed through further studies. Here, we provide new theoretical bases for the development of a new type of modulator that can reduce rice grain Cd content. The application of this modulator might ensure the quality and safety of rice in Cd-polluted farmland soils.
Cd pollution in farmland soils has become one of the most important agricultural environmental problems in China. In this study,the feasibility of 2,3-dimercaptosuccinic acid(DMSA)as a foliar modulator for the reduction of rice grain Cd content was evaluated. After spraying DMSA on rice leaves during flowering, we monitored the transport of Cd from phloem to grain. Moreover, we analyzed the effects of DMSA on the distribution of Cd and some other mineral elements in different parts of the rice, and discussed the mechanism through which DMSA could prevent the migration of Cd to the rice grains. The results showed that the application of DMSA on the leaf surface of late rice reduced the rice grain Cd content by 15.84%～46.09%; additionally, the Cd content in the rachis, the first internode, and the first node decreased by 10.03%～41.41%, 9.13%～28.46%, and 18.30%～38.32%, respectively. No significant difference in Cd content was noted in the other organs of the plant. The rice grain Cd content and the concentration of sprayed DMSA showed an obvious dose-effect relationship within a certain range; however, once the spraying concentration exceeded 4 mmol·L-1, the rice grain Cd content did not decrease continuously anymore. The results of this study can be used to support agricultural production. We further noticed that the foliar application of DMSA reduced the rice grain Mn content, but did not have significant effects on the content of other mineral elements(e.g. K, Mg, Ca, Fe,and Zn). After the application of DMSA, the transfer coefficient of Cd from the flag leaf to the first node of the plant was significantly reduced. The transfer coefficient of Cd from the first internode of the plants to the grains also showed a decreasing trend, but the reduction was not significant. According to the above results, the application of DMSA on rice leaves during flowering can reduce the transport of Cd to the grains, mainly through the chelation of Cd2+in the leaves and other tissues of the plant. The Mn content reduction in late rice grains,following the application of DMSA, might indicate that this acid affected the expression of gene Nramp5(a transporter of Cd and Mn); nevertheless, this hypothesis needs to be confirmed through further studies. Here, we provide new theoretical bases for the development of a new type of modulator that can reduce rice grain Cd content. The application of this modulator might ensure the quality and safety of rice in Cd-polluted farmland soils.
引文
[1] Rizwan M, Ali S, Akbar M Z, et al. Foliar application of aspartic acid lowers cadmium uptake and Cd-induced oxidative stress in rice under Cd stress[J]. Environmental Science and Pollution Research, 2017, 24(27):21938-21947.
[2] Liu F, Liu X N, Ding C, et al. The dynamic simulation of rice growth parameters under cadmium stress with the assimilation of multi-period spectral indices and crop model[J]. Field Crops Research, 2015, 183:225-234.
[3]陈能场,郑煜基,何晓峰,等.《全国土壤污染状况调查公报》探析[J].农业环境科学学报, 2017, 36(9):1689-1692.CHEN Neng-chang, ZHENG Yu-ji, HE Xiao-feng, et al. Analysis of the Report on the National General Survey of Soil Contamination[J].Journal of Agro-Environment Science, 2017, 36(9):1689-1692.
[4] Uraguchi S, Kamiya T, Sakamoto T, et al. Low-affinity cation transporter(OsLCT1)regulates cadmium transport into rice grains[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(52):20959-20964.
[5]中华人民共和国国家卫生和计划生育委员会国家食品药品监督管理总局.食品安全国家标准食品中污染物限量GB 2762—2017[S].北京：中国标准出版社, 2017.State Food and Drug Administration of the National Health and Family Planning Commission of the People′s Republic of China. National food safety standards for food contaminants GB 2762—2017[S]. Beijing:China Standards Press, 2017.
[6] Song Y, Wang Y, Mao W, et al. Dietary cadmium exposure assessment among the Chinese population[J]. PLoS One, 2017, 12(5):1-12.
[7] Kosolsaksakul P, Farmer J G, Oliver I W, et al. Geochemical associations and availability of cadmium(Cd)in a paddy field system, northwestern Thailand[J]. Environmental Pollution, 2014, 187:153-161.
[8] Clemens S, Ma J F. Toxic heavy metal and metalloid accumulation in crop plants and foods[J]. Annual Review of Plant Biology, 2016, 67(1):489-512.
[9]王梦梦,何梦媛,苏德纯.稻田土壤性质与稻米镉含量的定量关系[J].环境科学, 2018, 39(4):1918-1925.WANG Meng-meng, HE Meng-yuan, SU De-chun. Quantitative relationship between paddy soil properties and cadmium content in rice grains[J]. Environmental Science, 2018, 39(4):1918-1925.
[10] Liu Y, Zhang C, Zhao Y, et al. Effects of growing seasons and genotypes on the accumulation of cadmium and mineral nutrients in rice grown in cadmium contaminated soil[J]. Science of the Total Environment, 2017, 579:1282-1288.
[11]喻华,上官宇先,涂仕华,等.水稻籽粒中镉的来源[J].中国农业科学, 2018, 51(10):1940-1947.YU Hua, SHANGGUAN Yu-xian, TU Shi-hua, et al. Sources of cadmium accumulated in rice grain[J]. Scientia Agricultura Sinica, 2018,51(10):1940-1947.
[12]于焕云,崔江虎,乔江涛,等.稻田镉砷污染阻控原理与技术应用[J].农业环境科学学报, 2018, 37(7):1418-1426.YU Huan-yun, CUI Jiang-hu, QIAO Jiang-tao, et al. Principle and technique of arsenic and cadmium pollution control in paddy field[J].Journal of Agro-Environment Science, 2018, 37(7):1418-1426.
[13] Chen H, Zhang W, Yang X, et al. Effective methods to reduce cadmium accumulation in rice grain[J]. Chemosphere, 2018, 207:699-707.
[14]李义纯,王艳红,唐明灯,等.改良剂对根际土壤-水稻系统中镉运移的影响[J].环境科学, 2019. doi:10.13227/j.hjkx. 201811016.LI Yi-chun, WANG Yan-hong, TANG Ming-deng, et al. Effects of an amendment on cadmium transportation in rhizosphere soil-rice system[J]. Environmental Science, 2019. doi:10.13227/j. hjkx. 201811016.
[15] Uraguchi S, Mori S, Kuramata M. et al. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice[J]. Journal of Experimental Botany,2009, 60(9):2677-2688.
[16] Fujimaki S, Suzui N, Ishioka N S, et al. Tracing cadmium from culture to spikelet:Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant[J]. Plant Physiology, 2010, 152(4):1796-1806.
[17] Tanaka K, Fujimaki S, Fujiwara T, et al. Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants(Oryza sativa L.)[J]. Soil Science Plant and Nutrition, 2007, 53(1):72-77.
[18] Liu C P, Li F B, Luo C L, et al. Foliar application of two silica sols reduced cadmium accumulation in rice grains[J]. Journal of Hazardous Materials, 2009, 161(2/3):1466-1472.
[19] Chen R, Zhang C B, Zhao Y L, et al. Foliar application with nano-silicon reduced cadmium accumulation in grains by inhibiting cadmium translocation in rice plants[J]. Environmental Science and Pollution Research, 2018, 25(3):2361-2368.
[20] Gao M, Zhou J, Liu H L, et al. Foliar spraying with silicon and selenium reduces cadmium uptake and mitigates cadmium toxicity in rice[J]. Science of the Total Environment, 2018, 631/632:1100-1108.
[21]吕光辉,许超,王辉,等.叶面喷施不同浓度锌对水稻锌镉积累的影响[J].农业环境科学学报, 2018, 37(7):1521-1528.LüGuang-hui, XU Chao, WANG Hui, et al. Effect of foliar spraying zinc on the accumulation of zinc and cadmium in rice[J]. Journal of Agro-Environment Science, 2018, 37(7):1521-1528.
[22]尹晓辉,邹慧玲,方雅瑜,等.施锰方式对水稻吸收积累镉的影响研究[J].环境科学与技术, 2017, 40(8):8-12.YIN Xiao-hui, ZOU Hui-ling, FANG Ya-yu, et al. Effects of manganese fertilizer on absorption and accumulation of Cd in rice[J]. Environmental Science&Technology, 2017, 40(8):8-12.
[23]张烁,陆仲烟,唐琦,等.水稻叶面调理剂的降Cd效果及其对营养元素转运的影响[J].农业环境科学学报, 2018, 37(11):2507-2513.ZHANG Shuo, LU Zhong-yan, TANG Qi, et al. Effects of foliar modulators on cadmium accumulation and transport of nutrient elements in rice[J]. Journal of Agro-Environment Science, 2018, 37(11):2507-2513.
[24] Miller A L. Dimercaptosuccinic acid(DMSA), a non-toxic, water-soluble treatment for heavy metal toxicity[J]. Alternative Medicine Review, 1998, 3(3):199-207.
[25] Chisolm J J. Safety and efficacy of meso-2, 3-dimercaptosuccinic acid(DMSA)in children with elevated blood lead concentrations[J]. Journal of Toxicology. Clinical Toxicology, 2000, 38(4):365-2375.
[26] Kato M, Ishikawa S, Inagaki K, et al. Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants[J]. Soil Science and Plant Nutrition, 2010, 56:839-847.
[27]罗洁文,李莹,苏烁烁,等.类芦根系抗氧化酶和植物螯合肽对Cd、Pb胁迫的应答[J].生态环境学报, 2016, 25(6):1047-1053.LUO Jie-wen, LI Ying, SU Shuo-shuo, et al. Response of antioxidant enzymes and PCs in root of neyraudia-reynaudiana to Cd, Pb stress[J]. Ecology and Environment Sciences, 2016, 25(6):1047-1053.
[28]冯倩,台培东,付莎莎,等.巯基化合物在万寿菊镉解毒中的作用[J].环境工程学报, 2010, 4(1):214-218.FENG Qian, TAI Pei-dong, FU Sha-sha, et al. The role of thiol pool in cadmium detoxification in marigold plants[J]. Chinese Journal of Environmental Engineering, 2010, 4(1):214-218.
[29] Martinoia E, Grill E, Tommasini R. ATP-dependent glutathione Sconjugate‘export’pump in the vacuolar membrane of plants[J]. Nature, 1993, 364:247-249.
[30] Sasaki A, Yamaji N, Yokosho K, et al. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice[J]. The Plant Cell, 2012, 24(5):2155-2167.
[31] Ishikawa S, Ishimaru Y, Igura M, et al. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47):19166-19171.
[32] Tang L, Mao B G, Li Y K, et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield[J]. Scientific Reports, 2017, 7:14438.
[33] Fujimaki S, Suzui N, Ishioka N S, et al. Tracing cadmium from culture to spikelet:Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant[J]. Plant Physiology, 2010, 152(4):1796-1806.
[34] Kashiwagi T, Shindoh K, Hirotsu N, et al. Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant in rice[J]. BMC Plant Biology, 2009, 9:8.
[35] Yan Y F, Chio D W, Kim D, et al. Absorption, translocation, and remobilization of cadmium supplied at different growth stages of rice[J].Journal of Crop Science&Biotechnology, 2010, 13(2):113-119.
[36] Feng X M, Han L, Chao D Y, et al. Ionomic and transcriptomic analysis provides new insight into the distribution and transport of cadmium and arsenic in rice[J]. Journal of Hazardous Materials, 2017, 331:246-256.
[2] Liu F, Liu X N, Ding C, et al. The dynamic simulation of rice growth parameters under cadmium stress with the assimilation of multi-period spectral indices and crop model[J]. Field Crops Research, 2015, 183:225-234.
[3]陈能场,郑煜基,何晓峰,等.《全国土壤污染状况调查公报》探析[J].农业环境科学学报, 2017, 36(9):1689-1692.CHEN Neng-chang, ZHENG Yu-ji, HE Xiao-feng, et al. Analysis of the Report on the National General Survey of Soil Contamination[J].Journal of Agro-Environment Science, 2017, 36(9):1689-1692.
[4] Uraguchi S, Kamiya T, Sakamoto T, et al. Low-affinity cation transporter(OsLCT1)regulates cadmium transport into rice grains[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(52):20959-20964.
[5]中华人民共和国国家卫生和计划生育委员会国家食品药品监督管理总局.食品安全国家标准食品中污染物限量GB 2762—2017[S].北京：中国标准出版社, 2017.State Food and Drug Administration of the National Health and Family Planning Commission of the People′s Republic of China. National food safety standards for food contaminants GB 2762—2017[S]. Beijing:China Standards Press, 2017.
[6] Song Y, Wang Y, Mao W, et al. Dietary cadmium exposure assessment among the Chinese population[J]. PLoS One, 2017, 12(5):1-12.
[7] Kosolsaksakul P, Farmer J G, Oliver I W, et al. Geochemical associations and availability of cadmium(Cd)in a paddy field system, northwestern Thailand[J]. Environmental Pollution, 2014, 187:153-161.
[8] Clemens S, Ma J F. Toxic heavy metal and metalloid accumulation in crop plants and foods[J]. Annual Review of Plant Biology, 2016, 67(1):489-512.
[9]王梦梦,何梦媛,苏德纯.稻田土壤性质与稻米镉含量的定量关系[J].环境科学, 2018, 39(4):1918-1925.WANG Meng-meng, HE Meng-yuan, SU De-chun. Quantitative relationship between paddy soil properties and cadmium content in rice grains[J]. Environmental Science, 2018, 39(4):1918-1925.
[10] Liu Y, Zhang C, Zhao Y, et al. Effects of growing seasons and genotypes on the accumulation of cadmium and mineral nutrients in rice grown in cadmium contaminated soil[J]. Science of the Total Environment, 2017, 579:1282-1288.
[11]喻华,上官宇先,涂仕华,等.水稻籽粒中镉的来源[J].中国农业科学, 2018, 51(10):1940-1947.YU Hua, SHANGGUAN Yu-xian, TU Shi-hua, et al. Sources of cadmium accumulated in rice grain[J]. Scientia Agricultura Sinica, 2018,51(10):1940-1947.
[12]于焕云,崔江虎,乔江涛,等.稻田镉砷污染阻控原理与技术应用[J].农业环境科学学报, 2018, 37(7):1418-1426.YU Huan-yun, CUI Jiang-hu, QIAO Jiang-tao, et al. Principle and technique of arsenic and cadmium pollution control in paddy field[J].Journal of Agro-Environment Science, 2018, 37(7):1418-1426.
[13] Chen H, Zhang W, Yang X, et al. Effective methods to reduce cadmium accumulation in rice grain[J]. Chemosphere, 2018, 207:699-707.
[14]李义纯,王艳红,唐明灯,等.改良剂对根际土壤-水稻系统中镉运移的影响[J].环境科学, 2019. doi:10.13227/j.hjkx. 201811016.LI Yi-chun, WANG Yan-hong, TANG Ming-deng, et al. Effects of an amendment on cadmium transportation in rhizosphere soil-rice system[J]. Environmental Science, 2019. doi:10.13227/j. hjkx. 201811016.
[15] Uraguchi S, Mori S, Kuramata M. et al. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice[J]. Journal of Experimental Botany,2009, 60(9):2677-2688.
[16] Fujimaki S, Suzui N, Ishioka N S, et al. Tracing cadmium from culture to spikelet:Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant[J]. Plant Physiology, 2010, 152(4):1796-1806.
[17] Tanaka K, Fujimaki S, Fujiwara T, et al. Quantitative estimation of the contribution of the phloem in cadmium transport to grains in rice plants(Oryza sativa L.)[J]. Soil Science Plant and Nutrition, 2007, 53(1):72-77.
[18] Liu C P, Li F B, Luo C L, et al. Foliar application of two silica sols reduced cadmium accumulation in rice grains[J]. Journal of Hazardous Materials, 2009, 161(2/3):1466-1472.
[19] Chen R, Zhang C B, Zhao Y L, et al. Foliar application with nano-silicon reduced cadmium accumulation in grains by inhibiting cadmium translocation in rice plants[J]. Environmental Science and Pollution Research, 2018, 25(3):2361-2368.
[20] Gao M, Zhou J, Liu H L, et al. Foliar spraying with silicon and selenium reduces cadmium uptake and mitigates cadmium toxicity in rice[J]. Science of the Total Environment, 2018, 631/632:1100-1108.
[21]吕光辉,许超,王辉,等.叶面喷施不同浓度锌对水稻锌镉积累的影响[J].农业环境科学学报, 2018, 37(7):1521-1528.LüGuang-hui, XU Chao, WANG Hui, et al. Effect of foliar spraying zinc on the accumulation of zinc and cadmium in rice[J]. Journal of Agro-Environment Science, 2018, 37(7):1521-1528.
[22]尹晓辉,邹慧玲,方雅瑜,等.施锰方式对水稻吸收积累镉的影响研究[J].环境科学与技术, 2017, 40(8):8-12.YIN Xiao-hui, ZOU Hui-ling, FANG Ya-yu, et al. Effects of manganese fertilizer on absorption and accumulation of Cd in rice[J]. Environmental Science&Technology, 2017, 40(8):8-12.
[23]张烁,陆仲烟,唐琦,等.水稻叶面调理剂的降Cd效果及其对营养元素转运的影响[J].农业环境科学学报, 2018, 37(11):2507-2513.ZHANG Shuo, LU Zhong-yan, TANG Qi, et al. Effects of foliar modulators on cadmium accumulation and transport of nutrient elements in rice[J]. Journal of Agro-Environment Science, 2018, 37(11):2507-2513.
[24] Miller A L. Dimercaptosuccinic acid(DMSA), a non-toxic, water-soluble treatment for heavy metal toxicity[J]. Alternative Medicine Review, 1998, 3(3):199-207.
[25] Chisolm J J. Safety and efficacy of meso-2, 3-dimercaptosuccinic acid(DMSA)in children with elevated blood lead concentrations[J]. Journal of Toxicology. Clinical Toxicology, 2000, 38(4):365-2375.
[26] Kato M, Ishikawa S, Inagaki K, et al. Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants[J]. Soil Science and Plant Nutrition, 2010, 56:839-847.
[27]罗洁文,李莹,苏烁烁,等.类芦根系抗氧化酶和植物螯合肽对Cd、Pb胁迫的应答[J].生态环境学报, 2016, 25(6):1047-1053.LUO Jie-wen, LI Ying, SU Shuo-shuo, et al. Response of antioxidant enzymes and PCs in root of neyraudia-reynaudiana to Cd, Pb stress[J]. Ecology and Environment Sciences, 2016, 25(6):1047-1053.
[28]冯倩,台培东,付莎莎,等.巯基化合物在万寿菊镉解毒中的作用[J].环境工程学报, 2010, 4(1):214-218.FENG Qian, TAI Pei-dong, FU Sha-sha, et al. The role of thiol pool in cadmium detoxification in marigold plants[J]. Chinese Journal of Environmental Engineering, 2010, 4(1):214-218.
[29] Martinoia E, Grill E, Tommasini R. ATP-dependent glutathione Sconjugate‘export’pump in the vacuolar membrane of plants[J]. Nature, 1993, 364:247-249.
[30] Sasaki A, Yamaji N, Yokosho K, et al. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice[J]. The Plant Cell, 2012, 24(5):2155-2167.
[31] Ishikawa S, Ishimaru Y, Igura M, et al. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(47):19166-19171.
[32] Tang L, Mao B G, Li Y K, et al. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield[J]. Scientific Reports, 2017, 7:14438.
[33] Fujimaki S, Suzui N, Ishioka N S, et al. Tracing cadmium from culture to spikelet:Noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant[J]. Plant Physiology, 2010, 152(4):1796-1806.
[34] Kashiwagi T, Shindoh K, Hirotsu N, et al. Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant in rice[J]. BMC Plant Biology, 2009, 9:8.
[35] Yan Y F, Chio D W, Kim D, et al. Absorption, translocation, and remobilization of cadmium supplied at different growth stages of rice[J].Journal of Crop Science&Biotechnology, 2010, 13(2):113-119.
[36] Feng X M, Han L, Chao D Y, et al. Ionomic and transcriptomic analysis provides new insight into the distribution and transport of cadmium and arsenic in rice[J]. Journal of Hazardous Materials, 2017, 331:246-256.