Reviews and Special Topics

Research Advances on Molecular Genetic Mechanism for Cadmium Absorption and Transportation in Rice

Expand
  • State Key Laboratory for Rice Biology, China National Rice Research Institute, Hangzhou 310006, China;
*Corresponding author, E-mail: gaozhenyu@caas.cn

Received date: 2019-04-08

  Revised date: 2019-06-16

  Online published: 2019-09-10

Abstract

Cadmium is one of the heavy metals with serious toxicity to human health. The main source of cadmium in the human body is the consumption of rice with high levels of cadmium. Therefore, it is important to clarify the genetic mechanism of cadmium uptake, transport and accumulation in rice. So far, although the genetic pathway of cadmium accumulation has not been fully clarified in rice, the regulatory role of some genes in cadmium accumulation has been testified. Here, we briefly summarize the harm of cadmium stress on rice, the variation of cadmium accumulation among rice varieties, QTLs associated with cadmium accumulation in rice, genes related to cadmium absorption and transport, and application of them in rice breeding. Perspectives and research contents in the future were also advanced.

Cite this article

Shilin DING, Chaolei LIU, Qian QIAN, Zhenyu GAO . Research Advances on Molecular Genetic Mechanism for Cadmium Absorption and Transportation in Rice[J]. Chinese Journal OF Rice Science, 2019 , 33(5) : 383 -390 . DOI: 10.16819/j.1001-7216.2019.9040

References

[1] Clemens S, Aarts M G, Thomine S, Verbruggen N.Plant science: The key to preventing slow cadmium poisoning.Trends Plant Sci, 2013, 18(2): 92-99.
[2] Nawrot T S, Staessen J A, Roels H A, Munters E, Cuypers A, Richart T, Ruttens A, Smeets K, Clijsters H, Vangronsveld J.Cadmium exposure in the population: From health risks to strategies of prevention.Biometals, 2010, 23(5): 769-782.
[3] Satarug S, Garrett S H, Sens M A, Sens D A.Cadmium, environmental exposure, and health outcomes.Environ Health Perspect, 2010, 118(2): 182-190.
[4] Jarup L, Akesson A.Current status of cadmium as an environmental health problem.Toxicol Appl Pharmacol, 2009, 238(3): 201-208.
[5] Uraguchi S, Fujiwara T.Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation.Rice, 2012, 5(1): 5.
[6] 鄂志国, 张玉屏, 王磊. 水稻镉胁迫应答分子机制研究进展. 中国水稻科学, 2013, 27(5): 539-544.
[6] E Z G, Zhang Y P, Wang L. Molecular mechanism of rice responses to cadmium stress.Chin J Rice Sci, 2013, 27(5): 539-544. (in Chinese with English abstract)
[7] Yamagata N.Cadmium pollution in perspective.Bull Inst Public Heal, 1970, 19(1): 1-27.
[8] Yan J, Wang P, Wang P, Yang M, Lian X, Tang Z, Huang C F, Salt D E, Zhao F J.A loss-of-function allele ofOsHMA3 associated with high cadmium accumulation in shoots and grain of japonica rice cultivars. Plant Cell Environ, 2016, 39(9): 1941-1954.
[9] 易江, 甘平洋, 陈渠玲, 张源泉, 裴健儒, 黄天柱, 毛青秀, 陈昌勇. 稻米镉污染及其消减技术研究进展. 湖南农业科学, 2018, 390(3): 110-113.
[9] Yi J, Gan P Y, Chen Q L, Zhang Y Q,Pei J R,Huang T Z,Mao Q X,Chen C Y.Research progress on pollution of cadmium in rice and its removal technology.Hunan Agric Sci, 2018, 390(3): 110-113. (in Chinese with English abstract)
[10] 田艳芬, 史锟. 镉对水稻等作物的毒害作用. 垦殖与稻作, 2003(5): 26-28.
[10] Tian Y F, Shi K.Poisonous effects on rice and vegetables by cadmium.Reclaim Rice Cult, 2003(5): 26-28. (in Chinese with English abstract)
[11] 杨明, 陈璐, 徐庆国, 孙亚莉. 镉胁迫对不同水稻品种种子萌发和幼苗生长的影响. 作物研究, 2017, 31(6): 659-663.
[11] Yang M, Chen L, Xu Q G, Sun Y L.Effects of cadmium stress on seed germination and growth characteristic of different rice cultivars.Crop Res, 2017, 31(6): 659-663. (in Chinese with English abstract)
[12] 何俊瑜, 任艳芳, 严玉萍, 朱诚, 蒋德安. 镉胁迫对水稻幼苗生长和根尖细胞分裂的影响. 土壤学报, 2010, 47(1): 138-144.
[12] He J Y, Ren Y F, Yan Y P, Zhu C, Jiang D A.Impacts of cadmium stress on the growth of rice seedlings and division of their root tip cells.Acta Pedol Sin, 2010, 47(1): 138-144. (in Chinese with English abstract)
[13] 郭文燕, 田雄, 李尚锟, 李伟, 黄永相, 胡燕, 赵夏夏, 郭建夫. 镉胁迫对水稻光合生理特征及相关营养元素吸收影响研究. 安徽农业科学, 2018, 46(14): 37-43.
[13] Guo W Y, Tian X, Li S K, Li W, Huang Y X, Hu Y, Zhao X X, Guo J F.Effects of cadmium stress on the physiological and biochemical characters of rice at heading stage.J Anhui Agric Sci, 2018, 46(14): 37-43. (in Chinese with English abstract)
[14] 孙亚莉, 刘红梅, 徐庆国. 镉胁迫对不同水稻品种苗期光合特性与生理生化特性的影响. 华北农学报, 2017, 32(4): 176-181.
[14] Sun Y L, Liu H M, Xu Q G.Effect of cadmium stress on photosynthetic characteristics and physiological and biochemical traits during seedling stage of different rice cultivars.Acta Agric Boreali-Sin, 2017, 32(4): 176-181. (in Chinese with English abstract)
[15] Xue D W, Jiang H, Deng X X, Zhang X Q, Wang H, Xu X B, Hu J, Zeng D L, Guo L B, Qian Q.Comparative proteomic analysis provides new insights into cadmium accumulation in rice grain under cadmium stress.J Hazard Mater, 2014, 280: 269-278.
[16] Zhang X Q, Chen H N, Jiang H, Lu W, Pan J J, Qian Q, Xue D W.Measuring the damage of heavy metal cadmium in rice seedlings by SRAP analysis combined with physiological and biochemical parameters.J Sci Food Agric, 2015, 95(11): 2292-2298.
[17] 袁珍贵, 陈平平, 郭莉莉, 屠乃美, 易镇邪. 土壤镉含量影响水稻产量与稻穗镉累积分配的品种间差异. 作物杂志, 2018(1): 107-112.
[17] Yuan Z G, Chen P P, Guo L L, Tu N M, Yi Z X.Varietal difference in yield and Cd accumulation and distribution in panicle of rice affected by soil Cd content.Crops, 2018(1): 107-112. (in Chinese with English abstract)
[18] Arao T, Ae N.Genotypic variations in cadmium levels of rice grain.Soil Sci Plant Nutr, 2003, 49(4): 473-479.
[19] Liu J, Qian M, Cai G, Yang J, Zhu Q.Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain.J Hazard Mater, 2007, 143(1-2):443-447.
[20] Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma J F.A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol, 2009, 182(3): 644-653.
[21] Duan G, Shao G, Tang Z, Chen H, Wang B, Tang Z, Yang Y, Liu Y, Zhao F J.Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars.Rice, 2017, 10(1): 9.
[22] He J, Zhu C, Ren Y, Yan, Y, Jiang D. Genotypic variation in grain cadmium concentration of lowland rice.J Plant Nutr Soil Sci, 2006, 169(5): 711-716.
[23] Uraguchi S, Fujiwara T.Rice breaks ground for cadmium-free cereals.Curr Opin Plant Biol, 2013, 16(3): 328-334.
[24] Zhang X, Zhang G, Guo L B, Wang H Z, Zeng D L, Dong G J, Qian Q, Xue D W.Identification of quantitative trait loci for Cd and Zn concentrations of brown rice grown in Cd-polluted soils.Euphytica, 2011, 180(2): 173-179.
[25] Wang J H, Fang Y X, Tian B, Zhang X Q, Zeng D L, Guo L B, Hu J, Xue D W.New QTLs identified for leaf correlative traits in rice seedlings under cadmium stress.Plant Growth Regul, 2018, 85(2): 329-335.
[26] Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K.Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice.BMC Plant Biol, 2009, 9(1): 8.
[27] Ueno D, Koyama E, Kono I, Ando T, Yano M, Ma J F.Identification of a novel major quantitative trait locus controlling distribution of Cd between roots and shoots in rice.Plant Cell Physiol, 2009, 50(12): 2223-2233.
[28] Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S.Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice.J Exp Bot, 2009, 60(9): 2677-2688.
[29] Tezuka K, Miyadate H, Katou K, Kodama I, Matsumoto S, Kawamoto T, Masaki S, Satoh H, Yamaguchi M, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H.A single recessive gene controls cadmium translocation in the cadmium hyper- accumulating rice cultivar Cho-Ko-Koku.Theor Appl Genet, 2010, 120(6): 1175-1182.
[30] Ueno D, Yamaji N, Kono I, Huang C F, Ando T, Yano M, Ma J F.Gene limiting cadmium accumulation in rice.Proc Natl Acad Sci USA, 2010, 107(38): 16500-16505.
[31] Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H.OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles.New Phytol, 2011, 189(1): 190-199.
[32] Sasaki A, Yamaji N, Ma J F.Overexpression ofOsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot, 2014, 65(20): 6013-6021.
[33] Liu C L, Gao Z Y, Shang L G, Yang C H, Ruan B P, Zeng D L, Guo L B, Zhao F J, Huang C F, Qian Q.Natural variation in the promoter ofOsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice. J Integr Plant Biol, 2019, doi: 10.1111/jipb.12794.
[34] Sui F, Zhao D, Zhu H, Gong Y, Tang Z, Huang X Y, Zhang G, Zhao F J.Map-based cloning of a new total loss-of-function allele ofOsHMA3 causing high cadmium accumulation in rice grain. J Exp Bot, 2019, doi: 10.1093/jxb/erz093
[35] Huang Y, Sun C, Min J, Chen Y, Tong C, Bao J.Association mapping of quantitative trait loci for mineral element contents in whole grain rice (Oryza sativa L.). J Agric Food Chem, 2015, 63(50): 10885-10892.
[36] Sun L, Xu X, Jiang Y, Zhu Q, Yang F, Zhou J, Yang Y, Huang Z, Li A, Chen L, Tang W, Zhang G, Wang J, Xiao G, Huang D, Chen C.Genetic diversity, rather than cultivar type, determines relative grain Cd accumulation in hybrid rice.Front Plant Sci, 2016, 7: 1407.
[37] Xue D W, Chen M C, Zhang G P.Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica, 2009, 165(3): 587-596.
[38] Luo J S, Huang J, Zeng D L, Peng J S, Zhang G B, Ma H L, Guan Y, Yi H Y, Fu Y L, Han B, Lin H X, Qian Q, Gong J M.A defensin-like protein drives cadmium efflux and allocation in rice.Nat Commun, 2018, 9(1): 645.
[39] Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa N K, Nakanishi H.Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice.Proc Natl Acad Sci USA, 2012, 109(47): 19166-19171.
[40] Yan Y F, Lestari P, Lee K J, Kim M Y, Lee S H, Lee B W.Identification of quantitative trait loci for cadmium accumulation and distribution in rice (Oryza sativa). Genom, 2013, 56(4): 227-232.
[41] Liu W Q, Pan X W, Li Y C, Duan Y H, Min J, Liu S X, Liu L C, Sheng X N, Li X X.Identification of QTLs and validation ofqCd-2 associated with grain cadmium concentrations in rice . Rice Sci, 2019, 26(1): 42-49.
[42] Abe T, Nonoue Y, Ono N, Omoteno M, Kuramata M, Fukuoka S, Yamamoto T, Yano M, Ishikawa S.Detection of QTLs to reduce cadmium content in rice grains using LAC23/Koshihikari chromosome segment substitution lines.Breed Sci, 2013, 63(3): 284-291.
[43] Bughio N, Yamaguchi H, Nishizawa N K, Nakanishi H, Mori S.Cloning an iron-regulated metal transporter from rice.J Exp Bot, 2002, 53(374): 1677-1682.
[44] Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa N K.Iron deficiency enhances cadmium uptake and translocation mediated by the Fe transporters OsIRT1 and OSIRT2 in rice.Soil Sci Plant Nutr, 2006, 52(4): 464-469.
[45] Lee S, An G.Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice.Plant Cell Environ, 2009, 32(4): 408-416.
[46] Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K.The OsNRAMP1 iron transporter is involved in Cd accumulation in rice.J Exp Bot, 2011, 62(14): 4843-4850.
[47] Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K.Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport.Sci Rep, 2012, 2(6071): 286.
[48] Yang M, Zhang Y, Zhang L, Hu J, Zhang X, Lu K, Dong H, Wang D, Zhao F J, Huang C F, Lian X.OsNRAMP5 contributes to manganese translocation and distribution in rice shoots.J Exp Bot, 2014, 65(17): 4849-4861.
[49] Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X, Shao Y, Pan Y, Hu Y, Peng Y, Fu X, Li H, Xia S, Zhao B.Knockout ofOsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep, 2017, 7(1): 14 438.
[50] Clemens S, Ma J F.Toxic heavy metal and metalloid accumulation in crop plants and foods.Annu Rev Plant Biol, 2016, 67(1): 489-512.
[51] Lu C, Zhang L, Tang Z, Huang X Y, Ma J F, Zhao F J.Producing cadmium-freeIndica rice by overexpressing OsHMA3. Environ Int, 2019, 126: 619-626.
[52] Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa N K, Nakanishi H.The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice.Plant Cell Environ, 2012, 35(11): 1948-1957.
[53] Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H.Mutations in rice (Oryza sativa) heavy metal atpase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol, 2012, 53(1): 213-224.
[54] Hao X, Zeng M, Wang J, Zeng Z, Dai J, Xie Z, Yang Y, Tian L, Chen L, Li D.A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice.Front Plant Sci, 2018, 9: 476.
[55] Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T.Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains.Proc Natl Acad Sci USA, 2011, 108(52): 20 959-20 964.
[56] Uraguchi S, Kamiya T, Clemens S, Fujiwara T.Characterization of OsLCT1, a cadmium transporter fromindica rice. Physiol Plant, 2014, 151(3): 339-347.
[57] Zhao F Y, Han M M, Zhang S Y, Wang K, Zhang C R, Liu T, Liu W.Hydrogen peroxide-mediated growth of the root system occurs via auxin signaling modification and variations in the expression of cell-cycle genes in rice seedlings exposed to cadmium stress.J Integr Plant Biol, 2012, 54(12): 991-1006.
[58] Shimo H, Ishimaru Y, An G, Yamakawa T, Nakanishi H, Nishizawa N K.Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot, 2011, 62(15): 5727-5734.
[59] Lan H X, Wang Z F, Wang Q H, Wang M M, Bao Y M, Huang J, Zhang H S.Characterization of a vacuolar zinc transporter OZT1 in rice (Oryza sativa L.). Mol Biol Rep, 2013, 40(2): 1201-1210.
[60] Song W Y, Lee H S, Jin S R, Ko D, Martinoia E, Lee Y, An G, Ahn S N.Rice PCR1 influences grain weight and Zn accumulation in grains.Plant Cell Environ, 2015, 38(11): 2327-2339.
[61] Oda K, Otani M, Uraguchi S, Akihiro T, Fujiwara T.Rice ABCG43 is Cd inducible and confers cd tolerance on yeast.Biosci Biotechnol Biochem, 2011, 75(6): 1211-1213.
[62] 陈彩艳, 唐文帮. 筛选和培育镉低积累水稻品种的进展和问题探讨. 农业现代化研究, 2018, 39(6): 1044-1051.
[62] Chen C Y, Tang W B.A perspective on the selection and breeding of low-Cd rice.Res Agric Modern, 2018, 39(6): 1044-1051. (in Chinese with English abstract)
[63] Liu C L, Chen G, Li Y, Peng Y L, Zhang A P, Hong K, Jiang H Z, Ruan B P, Zhang B, Yang S L, Gao Z Y, Qian Q.Characterization of a major QTL for manganese accumulation in rice grain.Sci Rep, 2017, 7(1): 17704.
Outlines

/

Tel: 0571-63370278 E-mail: cjrs@263.net
Supported by Beijing Magtech Co., Ltd.