植物响应Cd胁迫研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2021-1286

摘要/Abstract

摘要：

镉（Cd）是一种毒性极强的重金属污染物,位于土壤无机污染物首位。Cd因具有强流动性和溶解性而容易被植物体吸收,不仅影响植物正常生理代谢并降低作物品质,还能通过食物链的传递和富集危害人体健康,因此植物对Cd胁迫的响应机制已成为研究的热点。本文综述了Cd胁迫对植物生理代谢和分子层次危害的同时,总结了植物在Cd胁迫下进化出的耐受性机制,以期为培育低积累作物和超积累Cd污染土壤修复植物提供理论依据。

关键词: Cd胁迫, 耐受性, 生理指标, 分子机制

Abstract:

Cadmium（Cd）is a heavy metal pollutant with heavy toxicity,ranking the first in soil inorganic pollutants. Cd can be absorbed by plants because of its strong fluidity and solubility. It affects the normal physiological metabolism of plants,reduces crop quality,and endangers human health through the transmission and enrichment of the food chain. Therefore,the response mechanism of plants to Cd stress has become a research hotspot. This paper reviews the damage effects of Cd stress on plant physiological metabolism and molecular level,and summarizes the tolerance mechanism that plants have evolved under Cd stress,aiming to provide a theoretical basis for cultivating low-accumulation crops and super-accumulation plants of remediating Cd contaminated soil.

Key words: Cd stress, tolerance, physiological index, molecular mechanism

刘自然, 甄珍, 陈强, 李玥莹, 王泽, 逄洪波. 植物响应Cd胁迫研究进展[J]. 生物技术通报, 2022, 38(6): 13-26.

LIU Zi-ran, ZHEN Zhen, CHEN Qiang, LI Yue-ying, WANG Ze, PANG Hong-bo. Research Progress in Plant Response to Cd Stress[J]. Biotechnology Bulletin, 2022, 38(6): 13-26.

图/表 2

图1 植物响应Cd胁迫的生理及分子机制 A：根际分泌物（主要包括高分子的植物螯合剂和金属硫蛋白以及低分子的H+、HCO3-、苹果酸和柠檬酸等）可以结合土壤中游离Cd并酸化根际土壤,是植物阻止Cd进入原生质体的第一道防线;B：植物阻止Cd进入原生质体的第二道防线是利用细胞壁结构物质纤维素、果胶和木质素固定Cd;C：由于植物细胞不具有Cd特异性转运蛋白,所以Cd2+必须与其他必需二价金属离子（如Fe2+/Ca2+/Mn2+）竞争转运蛋白（ZNT1、IRT1/2、NRAMP1/4及HMA4）从而进入原生质体;Cd进入细胞后可能与PCs（植物螯合肽）、MTs（金属硫蛋白）和NA（烟草胺）等螯合剂结合,转运蛋白可以将Cd及其螯合物转运至液泡（MTP1、YSL1、ABCC、YCF1、CAX1/2/4及HMA1/2/3）、叶绿体（ATM3及YSL6）及高尔基体（MTP11）中暂时储存,或排出细胞（PDF8）由木质部利用根压和蒸腾运输到地上部进行储存;D：抗氧化系统（酶类和非酶类系统）负责清除Cd毒害引发的大量活性氧,防止其扰乱细胞内部稳态平衡。酶类系统包括SOD（超氧化物歧化酶）、CAT（过氧化氢酶）、POD（过氧化物酶,peroxidase）、APX（抗坏血酸过氧化物酶）和GR（谷胱甘肽还原酶）,非酶类系统包括低质量的代谢物,如GSH（谷胱甘肽）、AsA（抗坏血酸）和脯氨酸等

Fig.1 Physiological and molecular mechanisms of plant response to Cd stress A：Rhizosphere exudates are the first line of defense for plants to prevent Cd from entering the protoplasm. It mainly includes high molecular weight plant chelating agents and metallothionein,as well as low molecular weight H+,HCO3-,malic acid and citric acid,etc. B：The second defense line for plants to prevent Cd from entering protoplasts is to fix Cd with cell wall structural materials cellulose,pectin and lignin. C：Cd2+ must compete with other essential divalent metal ions,such as Fe2+/Ca2+/Mn2+ for transporters（ZNT1,IRT1/2,NRAMP1/4 and HMA4）to enter the protoplast because there is no Cd-specific transporter in plant cells;Cd may bind to chelating agents such as PCs（phytochelatins）,MTs（metallothioneins）and NA（nicotinamide）after it enters the cell. Transport proteins can transport Cd and its chelates to the vacuole by MTP1,YSL1,ABCC,YCF1,CAX1/2/4 and HMA1/2/3,to chloroplasts by ATM3 and YSL6,and to Golgi by MTP11 temporarily stored,or Cd is excreted from cells by PDF8 and is transported from the xylem to the ground for storage using root pressure and transpiration. D：Antioxidant systems（such as enzymatic and non-enzymatic oxidants）are crucial for the detoxification of the ROS under stress conditions. It is responsible for preventing it from disturbing the homeostasis of cells. Enzymatic systems in plants include SOD（superoxide dismutase）,CAT（catalase from micrococcus lysodeiktic）,POD（peroxidase）,APX（ascorbate peroxidase）and GR（glutathione reductase）. The non-enzymatic antioxidant system includes low-mass metabolites like GSH（glutathione glutathione）,AsA（ascorbic acid）,and proline

图2 7种常见的重金属转运蛋白结构图直线：质膜和液泡膜等膜系统;长方形：跨膜结构域;曲线：跨膜区间。A：Zn/Fe转运蛋白（ZIP）;B：天然抗性相关巨噬细胞蛋白（NRAMP）;C：重金属ATP酶（HMA）;D：金属耐受蛋白（MTP）;E：阳离子交换体（CAX）;F：ATP结合盒转运蛋白（ABCC）,F1：ABCC半转运子,F2：ABCC全转运子;G：黄色条纹转运蛋白（YSL）

Fig.2 Structures of 7 common heavy metal transporters Straight line：Membrane systems such as plasma membrane and vacuolar membrane. Rectangle：Transmembrane domain. Curve：Transmembrane interval. A：Zinc and iron transporter proteins（ZIP）. B：Natural resistance-associated macrophage proteins（NRAMP）. C：Heavy metal ATPase（HMA）. D：Metal tolerance protein（MTP）. E：Cation exchanger（CAX）. F：ATP-binding cassette transporter（ABCC）;F1：ABCC semit ransporter;F2：ABCC full transporter. G：Yellow stripe-like transporter（YSL）

参考文献 105

[1]	赵中秋, 朱永官, 蔡运龙. 镉在土壤-植物系统中的迁移转化及其影响因素[J]. 生态环境, 2005, 14(2):282-286.
	Zhao ZQ, Zhu YG, Cai YL. Transport and transformation of cadmium in soil-plant systems and the influence factors[J]. Ecol Environ, 2005, 14(2):282-286.
[2]	Cailliatte R, Lapeyre B, Briat JF, et al. The NRAMP6 metal transporter contributes to cadmium toxicity[J]. Biochem J, 2009, 422(2):217-228. doi: 10.1042/BJ20090655 pmid: 19545236
[3]	林梅, 王湘平. 铅和镉胁迫对黄瓜种子萌发期间的毒害效应[J]. 湖南农业大学学报:自然科学版, 2012, 38(1):41-45.
	Lin M, Wang XP. Poison effect of Pb and Cd stress on cucumber seeds during the course of germination[J]. J Hunan Agric Univ:Nat Sci, 2012, 38(1):41-45.
[4]	吴恒梅, 纪艳, 姜成, 等. 重金属镉对丝瓜种子萌发及根系活力的影响[J]. 北方园艺, 2012(11):38-40.
	Wu HM, Ji Y, Jiang C, et al. Effects of heavy metal cadmium on seed germination and root activity of Luffa cylindrical[J]. North Hortic, 2012(11):38-40.
[5]	Chen J, Yang LB, Gu J, et al. MAN3 gene regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis thaliana[J]. New Phytol, 2015, 205(2):570-582. doi: 10.1111/nph.13101 URL
[6]	Gao J, Sun L, Yang XE, et al. Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance[J]. PLoS One, 2014, 8(6):e64643.
[7]	Dalcorso G, Fasani E, Furini A. Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics[J]. Front Plant Sci, 2013, 4:280.
[8]	Cuypers A, Plusquin M, Remans T, et al. Cadmium stress:an oxidative challenge[J]. Biometals, 2010, 23(5):927-940. doi: 10.1007/s10534-010-9329-x pmid: 20361350
[9]	Farmer EE, Mueller MJ. ROS-mediated lipid peroxidation and RES-activated signaling[J]. Annu Rev Plant Biol, 2013, 64:429-450. doi: 10.1146/annurev-arplant-050312-120132 URL
[10]	Srivastava S, Tripathi RD, Dwivedi UN. Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa—— an angiospermic parasite[J]. J Plant Physiol, 2004, 161(6):665-674. doi: 10.1078/0176-1617-01274 URL
[11]	Del Rio D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress[J]. Nutr Metab Cardiovasc Dis, 2005, 15(4):316-328. doi: 10.1016/j.numecd.2005.05.003 URL
[12]	龚双姣, 马陶武, 李菁, 等. 镉胁迫下三种藓类植物的细胞伤害及光合色素含量的变化[J]. 应用生态学报, 2010, 21(10):2671-2676.
	Gong SJ, Ma TW, Li J, et al. Leaf cell damage and changes in photosynthetic pigment contents of three moss species under cadmium stress[J]. Chin J Appl Ecol, 2010, 21(10):2671-2676.
[13]	Ma YL, Wang HF, Wang P, et al. Effects of cadmium stress on the antioxidant system and chlorophyll fluorescence characteristics of two Taxodium clones[J]. Plant Cell Rep, 2018, 37(11):1547-1555. doi: 10.1007/s00299-018-2327-0 URL
[14]	于方明, 汤叶涛, 仇荣亮, 等. Cd胁迫下超富集植物圆锥南芥抗氧化机理[J]. 环境科学学报, 2010, 30(2):409-414.
	Yu FM, Tang YT, Qiu RL, et al. Antioxidative responses to cadmium stress in the hyperaccumulator Arabis paniculata Franch[J]. J Environ Sci, 2010, 30(2):409-414.
[15]	张静, 赵秀侠, 汪翔, 等. 重金属镉(Cd)胁迫对水芹生长及生理特性的影响[J]. 植物生理学报, 2015, 51(11):1969-1974.
	Zhang J, Zhao XX, Wang X, et al. Effects of cadmium stress on the growth and physiological property of Oenanthe javanica[J]. Plant Physiol J, 2015, 51(11):1969-1974.
[16]	彭玲, 贾芬, 田小平, 等. 硒对油菜根尖镉胁迫的缓解作用[J]. 环境科学学报, 2015, 35(8):2597-2604.
	Peng L, Jia F, Tian XP, et al. Alleviation of cadmium stress on root tip of rape seedlings by selenium[J]. J Environ Sci, 2015, 35(8):2597-2604.
[17]	Wang H, Zhao SC, Liu RL, et al. Changes of photosynthetic activities of maize(Zea mays L.)seedlings in response to cadmium stress[J]. Photosynthetica, 2009, 47(2):277-283. doi: 10.1007/s11099-009-0043-2 URL
[18]	张义贤, 张丽萍. 重金属对大麦幼苗膜脂过氧化及脯氨酸和可溶性糖含量的影响[J]. 农业环境科学学报, 2006, 25(4):857-860.
	Zhang YX, Zhang LP. Effects of heavy metals on membrane lipid peroxidation, proline and soluble sugar in roots of Hordeum vulgare[J]. J Agro-Environ Sci, 2006, 25(4):857-860.
[19]	张丽萍, 刘志强, 金竹萍, 等. H₂S对镉胁迫下白菜幼苗根系渗透胁迫的调节作用[J]. 农业环境科学学报, 2016, 35(2):247-252.
	Zhang LP, Liu ZQ, Jin ZP, et al. Regulation of H₂S on Cd-induced osmotic stress in roots of Chinese cabbage seedling[J]. J Agro-Environ Sci, 2016, 35(2):247-252.
[20]	Zengin FK, Munzuroglu O. Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean(Phaseolus vulgaris L.)seedlings[J]. Acta Biologica Cracoviensia, 2005, 47(2):157-164.
[21]	覃光球, 严重玲, 韦莉莉. 秋茄幼苗叶片单宁、可溶性糖和脯氨酸含量对Cd胁迫的响应[J]. 生态学报, 2006, 26(10):3366-3371.
	Qin GQ, Yan CL, Wei LL. Effect of cadmium stress on the contents of tannin, soluble sugar and proline in Kandelia candel(L.)druce seedlings[J]. Acta Ecol Sin, 2006, 26(10):3366-3371.
[22]	Tripathi BN, Gaur JP. Physiological behavior of Scenedesmus sp. during exposure to elevated levels of Cu and Zn and after withdrawal of metal stress[J]. Protoplasma, 2006, 229(1):1-9. pmid: 17102929
[23]	Liu D, Jiang W, Gao X. Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic[J]. Biol Plant, 2003, 47(1):79-83.
[24]	葛才林, 杨小勇, 孙锦荷, 等. 重金属胁迫引起的水稻和小麦幼苗DNA损伤[J]. 植物生理与分子生物学学报, 2002, 28(6):419-424.
	Ge CL, Yang XY, Sun JH, et al. DNA damage caused by heavy metal stress in rice and wheat seedlings[J]. J Plant Physiol Mol Biol, 2002, 28(6):419-424.
[25]	张旭红, 林爱军, 苏玉红, 等. 镉引起蚕豆(Vicia faba)叶片DNA损伤和细胞凋亡研究[J]. 环境科学, 2006, 27(4):787-793.
	Zhang XH, Lin AJ, Su YH, et al. DNA damages and apoptosis induced by Cd in the leaves of horsebean Vicia faba[J]. Environ Sci, 2006, 27(4):787-793.
[26]	吕朝晖, 王焕校. 镉铅对小麦醇脱氢酶(ADH)基因表达影响的初步研究[J]. 环境科学学报, 1998, 18(5):500-503
	Lv CH, Wang HX. Effects of cadmium and lead on adh gene experssion[J]. J Environ Sci, 1998, 18(5):500-503
[27]	刘宛, 郑乐, 李培军, 等. 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, 2006, 25(1):19-24.
	Liu W, Zheng L, Li PJ, et al. Effects of cadmium stress on DNA polymorphism of genome in barley seedlings[J]. J Agro-Environ Sci, 2006, 25(1):19-24.
[28]	曹继敏, 李双财, 何德. 镉胁迫后旱柳转录组变化分析[J]. 生物技术通报, 2020(7):32-39. doi: 10.13560/j.cnki.biotech.bull.1985.2019-1018
	Cao JM, Li SC, He D. Transcriptome analysis of Saliz matsudana under cadmium stress[J]. Biotechnol Bull, 2020, 36(7):32-39.
[29]	Xu J, Sun JH, Du LG, et al. Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum[J]. New Phytol, 2012, 196(1):110-124. doi: 10.1111/j.1469-8137.2012.04235.x URL
[30]	何其浩, 周韬, 孙吉康, 等. 镉胁迫对栾树幼苗不同组织部位转录组差异研究[J]. 环境科学学报, 2021. https://doi.org/10.13671/j.hjkxxb.2021.0397.
	He QH, Zhou T, Sun JK, et al. Effect of cadmium stress on transcriptome differences in roots and leaves of Koelreuteria paniculata seedlings[J]. J Environ Sci, 2021. https://doi.org/10.13671/j.hjkxxb.2021.0397.
[31]	赵春. Cd²⁺胁迫对石龙尾超微结构的影响[J]. 广西植物, 2008, 28(5):592-595.
	Zhao C. Effect of Cd²⁺ stress on ultrastructure of Limnophila sessiliflora[J]. Guihaia, 2008, 28(5):592-595.
[32]	Sormani R, Delannoy E, Lageix S, et al. Sublethal cadmium intoxication in Arabidopsis thaliana impacts translation at multiple levels[J]. Plant Cell Physiol, 2011, 52(2):436-447. doi: 10.1093/pcp/pcr001 pmid: 21252299
[33]	江行玉, 赵可夫. 植物重金属伤害及其抗性机理[J]. 应用与环境生物学报, 2001, 7(1):92-99.
	Jiang XY, Zhao KF. Mechanism of heavy metal injury and resistance of plants[J]. Chin J Appl Environ Biol, 2001, 7(1):92-99.
[34]	李荣春. Cd、Pb及其复合污染对烤烟叶片生理生化及细胞亚显微结构的影响[J]. 植物生态学报, 2000, 24(2):238-242.
	Li RC. Effects of cadmium and lead on physiological and ultra-structural features in tobacco leaves[J]. Chin J Plant Ecol, 2000, 24(2):238-242.
[35]	肖清铁, 戎红, 周丽英, 等. 水稻叶片对镉胁迫响应的蛋白质差异表达[J]. 应用生态学报, 2011, 22(4):1013-1019.
	Xiao QT, Rong H, Zhou LY, et al. Differential expression of proteins in Oryza sativa leaves in response to cadmium stress[J]. Chin J Appl Ecol, 2011, 22(4):1013-1019.
[36]	孟玲, 王焕校, 谭德勇. 云南会泽铅锌矿污染导致小麦种子蛋白基因表达的变化[J]. 作物学报, 1998, 24(3):375-379.
	Meng L, Wang HX, Tan DY. The alteration of gene exp ression of wheat seed proteins by mineral pollution of lead and zinc in Huize, Yunnan Province[J]. Acta Agron Sin, 1998, 24(3):375-379.
[37]	Chen H, Li Y, Ma X, et al. Analysis of potential strategies for cadmium stress tolerance revealed by transcriptome analysis of upland cotton[J]. Sci Rep, 2019, 9(1):86. doi: 10.1038/s41598-018-36228-z URL
[38]	Michalek JL, Lee SJ, Michel SL. Cadmium coordination to the zinc binding domains of the non-classical zinc finger protein Tristetraprolin affects RNA binding selectivity[J]. J Inorg Biochem, 2012, 112:32-38. doi: 10.1016/j.jinorgbio.2012.02.023 pmid: 22542594
[39]	能凤娇, 刘鸿雁, 马莹, 等. 根际促生菌在植物修复重金属污染土壤中的应用研究进展[J]. 中国农学通报, 2013, 29(5):187-191.
	Neng FJ, Liu HY, Ma Y, et al. Research progress on the applications of plant growth-promoting rhizobacteria in phytoremediation of heavy metals-contaminated soil[J]. Chin Agric Sci Bull, 2013, 29(5):187-191.
[40]	廉梅花, 孙丽娜, 胡筱敏, 等. pH对不同富集能力植物根际土壤溶液中镉形态的影响[J]. 生态学杂志, 2015, 34(1):130-137.
	Lian MH, Sun LN, Hu XM, et al. Effect of pH on cadmium speciation in rhizosphere soil solutions of different cadmium accumulating plants[J]. Chin J Ecol, 2015, 34(1):130-137.
[41]	Lu HL, Yan CL, Liu JC. Low-molecular-weight organic acids exuded by Mangrove(Kandelia candel(L.)Druce)roots and their effect on cadmium species change in the rhizosphere[J]. Environ Exp Bot, 2007, 61(2):159-166. doi: 10.1016/j.envexpbot.2007.05.007 URL
[42]	Malovíková A, Kohn R. Binding of cadmium cations to pectin[J]. Collect Czech Chem Commun, 1982, 47(2):702-708. doi: 10.1135/cccc19820702 URL
[43]	Wang MQ, Bai ZY, Xiao YF, et al. Transcriptomic analysis of Verbena bonariensis roots in response to cadmium stress[J]. BMC Genom, 2019, 20(1):1-14. doi: 10.1186/s12864-018-5379-1 URL
[44]	Wang P, Yang B, Wan HB, et al. The differences of cell wall in roots between two contrasting soybean cultivars exposed to cadmium at young seedlings[J]. Environ Sci Pollut Res Int, 2018, 25(29):29705-29714. doi: 10.1007/s11356-018-2956-4 URL
[45]	Wójcik M, Skórzyńska-Polit E, Tukiendorf A. Organic acids accumulation and antioxidant enzyme activities in Thlaspi caerulescens under Zn and Cd stress[J]. Plant Growth Regul, 2006, 48(2):145-155. doi: 10.1007/s10725-005-5816-4 URL
[46]	Hendrix S, Jozefczak M, Wójcik M, et al. Glutathione:a key player in metal chelation, nutrient homeostasis, cell cycle regulation and the DNA damage response in cadmium-exposed Arabidopsis thaliana[J]. Plant Physiol Biochem, 2020, 154:498-507. doi: 10.1016/j.plaphy.2020.06.006 URL
[47]	Li JC, Guo JB, Xu WZ, et al. RNA interference-mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds[J]. J Integr Plant Biol, 2007, 49(7):1032-1037. doi: 10.1111/j.1672-9072.2007.00473.x URL
[48]	Clemens S. Molecular mechanisms of plant metal tolerance and homeostasis[J]. Planta, 2001, 212(4):475-486. pmid: 11525504
[49]	Martínez M, Bernal P, Almela C, et al. An engineered plant that accumulates higher levels of heavy metals than Thlaspi caerulescens, with yields of 100 times more biomass in mine soils[J]. Chemosphere, 2006, 64(3):478-485. pmid: 16337669
[50]	Howden R, Goldsbrough PB, Andersen CR, et al. Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient[J]. Plant Physiol, 1995, 107(4):1059-1066. pmid: 7770517
[51]	Du J, Yang JL, Li CH, et al. Advances in metallotionein studies in forest trees[J]. Plant Omics, 2012, 5(1):46-51.
[52]	Misra S, Gedamu L. Heavy metal tolerant transgenic Brassica napus L. and Nicotiana tabacum L. plants[J]. Theor Appl Genet, 1989, 78(2):161-168. doi: 10.1007/BF00288793 pmid: 24227139
[53]	Murphy A, Zhou J, Goldsbrough PB, et al. Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana[J]. Plant Physiol, 1997, 113(4):1293-1301. pmid: 9112777
[54]	Khafi AS, Iranbakhsh A, Safipour Afshar A, et al. RBOH expression and ROS metabolism in Citrullus colocynthis under cadmium stress[J]. Braz J Bot, 2020, 43(1):35-43. doi: 10.1007/s40415-020-00581-z URL
[55]	Siddiqui MH, Al-Whaibi MH, Sakran AM, et al. Effect of calcium and potassium on antioxidant system of Vicia faba L. Under cadmium stress[J]. Int J Mol Sci, 2012, 13(6):6604-6619. doi: 10.3390/ijms13066604 pmid: 22837652
[56]	张玉秀, 金玲, 冯珊珊, 等. 镉对镉超累积植物龙葵抗氧化酶活性及基因表达的影响[J]. 中国科学院研究生院学报, 2013, 30(1):11-17.
	Zhang YX, Jin L, Feng SS, et al. Effects of Cd on activity and gene expression of antioxidant enzymes in hyperaccumulator Solanum nigrum L[J]. J Grad Univ Chin Acad Sci, 2013, 30(1):11-17.
[57]	司廉邦. 茶多酚对盐胁迫下小麦生理特性及抗氧化系统相关基因表达的影响[D]. 兰州: 西北师范大学, 2019.
	Si LB. Effects of tea polyphenols on physiological characteristics and antioxidant system related gene expression in wheat under salt stress[D]. Lanzhou: Northwest Normal University, 2019.
[58]	Kim KH, Kim YN, Lim GH, et al. Expression of catalase(CAT)and ascorbate peroxidase(APX)in MuSI transgenic tobacco under cadmium stress[J]. Korean J Soil Sci Fertil, 2011, 44(1):53-57. doi: 10.7745/KJSSF.2011.44.1.053 URL
[59]	Bowers K, Srai SKS. The trafficking of metal ion transporters of the Zrt- and Irt-like protein family[J]. Traffic, 2018, 19(11):813-822. doi: 10.1111/tra.12602 URL
[60]	Verbruggen N, Hermans C, Schat H. Molecular mechanisms of metal hyperaccumulation in plants[J]. New Phytol, 2009, 181(4):759-776. doi: 10.1111/j.1469-8137.2008.02748.x pmid: 19192189
[61]	Lin YF, Hassan Z, Talukdar S, et al. Expression of the ZNT1 zinc transporter from the metal hyperaccumulator Noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana[J]. PLoS One, 2016, 11(3):e0149750.
[62]	Zhu XF, Jiang T, Wang ZW, et al. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana[J]. J Hazard Mater, 2012, (15):302-307.
[63]	Nakanishi H, Ogawa I, Ishimaru Y, et al. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe²⁺ transporters OsIRT1 and OsIRT2 in rice[J]. Soil Sci Plant Nutr, 2006, 52(4):464-469. doi: 10.1111/j.1747-0765.2006.00055.x URL
[64]	Harrison C, Katayama S, Dhut S, et al. SCFPof1-ubiquitin and its target Zip1 transcription factor mediate cadmium response in fission yeast[J]. EMBO J, 2005, 24(3):599-610. doi: 10.1038/sj.emboj.7600536 pmid: 15660136
[65]	Wu X, Zhu ZB, Chen JH, et al. Transcriptome analysis revealed pivotal transporters involved in the reduction of cadmium accumulation in pak choi(Brassica chinensis L.)by exogenous hydrogen-rich water[J]. Chemosphere, 2019, 216:684-697. doi: 10.1016/j.chemosphere.2018.10.152 URL
[66]	马晓晓. 锌/镉超积累植物东南景天(Sedum alfredii Hance L.)两个锌转运蛋白基因的功能研究[D]. 杭州: 浙江大学, 2015.
	Ma XX. Functional analysis of two zinc transporters from the Zn/Cd hvperaccumulator Sedum alfredii Hance[D]. Hangzhou: Zhejiang University, 2015.
[67]	Zeng L, Zhu T, Gao Y, et al. Effects of Ca addition on the uptake, translocation, and distribution of Cd in Arabidopsis thaliana[J]. Ecotoxicol Environ Saf, 2017, 139:228-237. doi: 10.1016/j.ecoenv.2017.01.023 URL
[68]	Kavitha PG, Kuruvilla S, Mathew MK. Functional characterization of a transition metal ion transporter, OsZIP 6 from rice(Oryza sativa L.)[J]. Plant Physiol Biochem, 2015, 97:165-174. doi: 10.1016/j.plaphy.2015.10.005 URL
[69]	职帅, 李畅, 陈景光, 等. 锌铁转运蛋白基因OsZIP5和Os-ZIP9参与水稻Zn²⁺和Cd²⁺的吸收和转运[J]. 分子植物育种, 2021, 19(1):137-148.
	Zhi S, Li C, Chen JG, et al. Zinc-iron transporter genes OsZIP5 and OsZIP9 are involved in the uptake and transport of Zn²⁺ and Cd²⁺ in rice[J]. Mol Plant Breed, 2021, 19(1):137-148.
[70]	Fujishiro H, Okugaki S, Yasumitsu S, et al. Involvement of DNA hypermethylation in down-regulation of the zinc transporter ZIP8 in cadmium-resistant metallothionein-null cells[J]. Toxicol Appl Pharmacol, 2009, 241(2):195-201. doi: 10.1016/j.taap.2009.08.015 URL
[71]	Nevo Y, Nelson N. The NRAMP family of metal-ion transporters[J]. Biochim et Biophys Acta BBA Mol Cell Res, 2006, 1763(7):609-620.
[72]	Bozzi AT, Bane LB, Weihofen WA, et al. Conserved methionine dictates substrate preference in Nramp-family divalent metal transporters[J]. PNAS, 2016, 113(37):10310-10315. doi: 10.1073/pnas.1607734113 URL
[73]	陈可欣. 黄瓜Cd低积累品种筛选和Cd积累机理研究[D]. 杭州: 浙江农林大学, 2019.
	Chen KX. Study on Cd accumulation mechanism and selection of cultivars with low Cd accumulation in cucumber[D]. Hangzhou: Zhejiang A & F University, 2019.
[74]	Li Y, Qin Y, Xu W, et al. Differences of Cd uptake and expression of MT family genes and NRAMP2 in two varieties of ryegrasses[J]. Environ Sci Pollut Res Int, 2019, 26(14):13738-13745. doi: 10.1007/s11356-018-2649-z URL
[75]	Thomine S, Wang R, Ward JM, et al. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes[J]. PNAS, 2000, 97(9):4991-4996. pmid: 10781110
[76]	Sasaki A, Yamaji N, Yokosho K, et al. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice[J]. Plant Cell, 2012, 24(5):2155-2167. doi: 10.1105/tpc.112.096925 URL
[77]	Migeon A, Blaudez D, Wilkins O, et al. Genome-wide analysis of plant metal transporters, with an emphasis on poplar[J]. Cell Mol Life Sci, 2010, 67(22):3763-3784. doi: 10.1007/s00018-010-0445-0 pmid: 20623158
[78]	Smith AT, Smith KP, Rosenzweig AC. Diversity of the metal-transporting P1B-type ATPases[J]. J Biol Inorg Chem, 2014, 19(6):947-960. doi: 10.1007/s00775-014-1129-2 URL
[79]	Zhao HX, Wang LS, Zhao FJ, et al. SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola[J]. Plant Cell Environ, 2018, 42(4):1112-1124. doi: 10.1111/pce.13456 URL
[80]	Satoh-Nagasawa N, Mori M, Nakazawa N, et al. Mutations in rice(Oryza sativa)heavy metal ATPase 2(OsHMA2)restrict the translocation of zinc and cadmium[J]. Plant Cell Physiol, 2012, 53(1):213-224. doi: 10.1093/pcp/pcr166 pmid: 22123790
[81]	Park W, Ahn SJ. HMA3 is a key factor for differences in Cd- and Zn-related phenotype between Arabidopsis Ws and Col-0 ecotypes[J]. Plant Biotechnol Rep, 2017, 11(4):209-218. doi: 10.1007/s11816-017-0447-6 URL
[82]	Grispen VMJ, Hakvoort HWJ, Bliek T, et al. Combined expression of the Arabidopsis metallothionein MT2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco[J]. Environ Exp Bot, 2011, 72(1):71-76. doi: 10.1016/j.envexpbot.2010.01.005 URL
[83]	Guo H, Hong C, Xiao M, et al. Real-time kinetics of cadmium transport and transcriptomic analysis in low cadmium accumulator Miscanthus sacchariflorus[J]. Planta, 2016, 244(6):1289-1302. doi: 10.1007/s00425-016-2578-3 URL
[84]	Lu M, Fu D. Structure of the zinc transporter YiiP[J]. Sci, 2007, 317(5845):1746-1748.
[85]	Lu M, Chai J, Fu D. Structural basis for autoregulation of the zinc transporter YiiP[J]. Nat Struct Mol Biol, 2009, 16(10):1063-1067. doi: 10.1038/nsmb.1662 URL
[86]	Das N, Bhattacharya S, Maiti MK. Enhanced cadmium accumulation and tolerance in transgenic tobacco overexpressing rice metal tolerance protein gene OsMTP1 is promising for phytoremediation[J]. Plant Physiol Biochem, 2016, 105:297-309. doi: 10.1016/j.plaphy.2016.04.049 URL
[87]	Peiter E, Montanini B, Gobert A, et al. A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance[J]. PNAS, 2007, 104(20):8532-8537. pmid: 17494768
[88]	Ma G, Li JY, Li JJ, et al. OsMTP11, a trans-Golgi network localized transporter, is involved in manganese tolerance in rice[J]. Plant Sci, 2018, 274:59-69. doi: 10.1016/j.plantsci.2018.05.011 URL
[89]	Shigaki T, Rees I, Nakhleh L, et al. Identification of three distinct phylogenetic groups of CAX cation/proton antiporters[J]. J Mol Evol, 2006, 63(6):815-825. pmid: 17086450
[90]	Korenkov V, Hirschi K, Crutchfield JD, et al. Enhancing tonoplast Cd/H antiport activity increases Cd, Zn, and Mn tolerance, and impacts root/shoot Cd partitioning in Nicotiana tabacum L[J]. Planta, 2007, 226(6):1379-1387. pmid: 17636324
[91]	Pittman JK, Shigaki T, Marshall JL, et al. Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter[J]. Plant Mol Biol, 2004, 56(6):959-971. pmid: 15821993
[92]	Wu QY, Shigaki T, Williams KA, et al. Expression of an Arabidopsis Ca²⁺/H⁺ antiporter CAX1 variant in Petunia enhances cadmium tolerance and accumulation[J]. J Plant Physiol, 2011, 168(2):167-173. doi: 10.1016/j.jplph.2010.06.005 URL
[93]	Hirschi KD, Korenkov VD, Wilganowski NL, et al. Expression of Arabidopsis CAX2 in tobacco altered metal accumulation and increased manganese tolerance[J]. Plant physiol, 2000, 124(1):125-134. pmid: 10982428
[94]	Mei H, Cheng NH, Zhao J, et al. Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4[J]. New Phytol, 2009, 183(1):95-105. doi: 10.1111/j.1469-8137.2009.02831.x URL
[95]	郜红建, 广敏, 徐佳佳, 等. ABC转运蛋白介导离子跨膜运输的研究进展[J]. 安徽农业大学学报, 2019, 46(3):491-495.
	Gao HJ, Guang M, Xu JJ, et al. Research progress of ABC transporter mediated ion transmembrane transportation[J]. J Anhui Agric Univ, 2019, 46(3):491-495.
[96]	Sánchez-Fernández R, Davies TG, Coleman JO, et al. The Arabidopsis thaliana ABC protein superfamily, a complete inventory[J]. J Biol Chem, 2001, 276(32):30231-30244. doi: 10.1074/jbc.M103104200 pmid: 11346655
[97]	Bhuiyan MSU, Min SR, Jeong WJ, et al. Overexpression of a yeast cadmium factor 1(YCF₁)enhances heavy metal tolerance and accumulation in Brassica juncea[J]. Plant Cell Tissue Org, 2011, 105(1):85-91. doi: 10.1007/s11240-010-9845-y URL
[98]	Brunetti P, Zanella L, De Paolis A, et al. Cadmium-inducible expression of the ABC-type transporter AtABCC₃ increases phytochelatin-mediated cadmium tolerance in Arabidopsis[J]. J Exp Bot, 2015, 66(13):3815-3829. doi: 10.1093/jxb/erv185 URL
[99]	Gaillard S, Jacquet H, Vavasseur A, et al. AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana[J]. BMC Plant Biol, 2008, 8:22. doi: 10.1186/1471-2229-8-22 URL
[100]	Sheng YB, Yan XB, Huang Y, et al. The WRKY transcription factor, WRKY13, activates PDR8 expression to positively regulate cadmium tolerance in Arabidopsis[J]. Plant Cell Environ, 2018, 42(3):891-903. doi: 10.1111/pce.13457 URL
[101]	Kim DY, Bovet L, Kushnir S, et al. AtATM3 is involved in heavy metal resistance in Arabidopsis[J]. Plant Physiol, 2006, 140(3):922-932. doi: 10.1104/pp.105.074146 URL
[102]	Schaaf G, Ludewig U, Erenoglu BE, et al. ZmYSL1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals[J]. J Biol Chem, 2004, 279(10):9091-9096. doi: 10.1074/jbc.M311799200 URL
[103]	Feng S, Tan J, Zhang Y, et al. Isolation and characterization of a novel cadmium-regulated yellow stripe-like transporter(SnYS-L3)in Solanum nigrum[J]. Plant Cell Rep, 2017, 36(2):281-296. doi: 10.1007/s00299-016-2079-7 URL
[104]	Chen SP, Liu YS, Deng Y, et al. Cloning and functional analysis of the VcCXIP4 and VcYSL6 genes as Cd-regulating genes in blueberry[J]. Gene, 2019, 686:104-117. doi: 10.1016/j.gene.2018.10.078 URL
[105]	Zhang XD, Meng JG, Zhao KX, et al. Annotation and characterization of Cd-responsive metal transporter genes in rapeseed(Brassica napus)[J]. Biometals, 2018, 31(1):107-121. doi: 10.1007/s10534-017-0072-4 pmid: 29250721