Full Text:   <1275>

Summary:  <1035>

CLC number: S184

On-line Access: 2020-06-01

Received: 2019-09-30

Revision Accepted: 2020-01-15

Crosschecked: 2020-05-25

Cited: 0

Clicked: 2025

Citations:  Bibtex RefMan EndNote GB/T7714


Fei-Bo Wu


-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2020 Vol.21 No.6 P.442-459


Breeding for low cadmium accumulation cereals

Author(s):  Qin Chen, Fei-Bo Wu

Affiliation(s):  Department of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China

Corresponding email(s):   wufeibo@zju.edu.cn

Key Words:  Cereals, Low Cd accumulation, Gene/quantitative trait locus (QTL) mapping, Breeding

Qin Chen, Fei-Bo Wu. Breeding for low cadmium accumulation cereals[J]. Journal of Zhejiang University Science B, 2020, 21(6): 442-459.

@article{title="Breeding for low cadmium accumulation cereals",
author="Qin Chen, Fei-Bo Wu",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Breeding for low cadmium accumulation cereals
%A Qin Chen
%A Fei-Bo Wu
%J Journal of Zhejiang University SCIENCE B
%V 21
%N 6
%P 442-459
%@ 1673-1581
%D 2020
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1900576

T1 - Breeding for low cadmium accumulation cereals
A1 - Qin Chen
A1 - Fei-Bo Wu
J0 - Journal of Zhejiang University Science B
VL - 21
IS - 6
SP - 442
EP - 459
%@ 1673-1581
Y1 - 2020
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1900576

Cadmium (Cd) is an element that is nonessential and extremely toxic to both plants and human beings. Soil contaminated with Cd has adverse impacts on crop yields and threatens human health via the food chain. Cultivation of low-Cd cultivars has been of particular interest and is one of the most cost-effective and promising approaches to minimize human dietary intake of Cd. Low-Cd crop cultivars should meet particular criteria, including acceptable yield and quality, and their edible parts should have Cd concentrations below maximum permissible concentrations for safe consumption, even when grown in Cd-contaminated soil. Several low-Cd cereal cultivars and genotypes have been developed worldwide through cultivar screening and conventional breeding. Molecular markers are powerful in facilitating the selection of low-Cd cereal cultivars. Modern molecular breeding technologies may have great potential in breeding programs for the development of low-Cd cultivars, especially when coupled with conventional breeding. In this review, we provide a synthesis of low-Cd cereal breeding.



Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Abe T, Taguchi-Shiobara F, Kojima Y, et al., 2011. Detection of a QTL for accumulating Cd in rice that enables efficient Cd phytoextraction from soil. Breed Sci, 61(1):43-51.

[2]Abe T, Nonoue Y, Ono N, et al., 2013. Detection of QTLs to reduce cadmium content in rice grains using LAC23/ Koshihikari chromosome segment substitution lines. Breed Sci, 63(3):284-291.

[3]AbuHammad WA, Mamidi S, Kumar A, et al., 2016. Identification and validation of a major cadmium accumulation locus and closely associated SNP markers in North Dakota durum wheat cultivars. Mol Breed, 36(8):112.

[4]Ansarypour Z, Shahpiri A, 2017. Heterologous expression of a rice metallothionein isoform (OsMTI-1b) in Saccharomyces cerevisiae enhances cadmium, hydrogen peroxide and ethanol tolerance. Braz J Microbiol, 48(3):537-543.

[5]Aprile A, Sabella E, Vergine M, et al., 2018. Activation of a gene network in durum wheat roots exposed to cadmium. BMC Plant Biol, 18:238.

[6]Arao T, Ae N, 2003. Genotypic variations in cadmium levels of rice grain. Soil Sci Plant Nutr, 49(4):473-479.

[7]Arduini I, Masoni A, Mariotti M, et al., 2014. Cadmium uptake and translocation in durum wheat varieties differing in grain-Cd accumulation. Plant Soil Environ, 60(1):43-49.


[9]Arthur E, Crews H, Morgan C, 2000. Optimizing plant genetic strategies for minimizing environmental contamination in the food chain. Int J Phytoremediation, 2(1):1-21.

[10]Arunakumara KKIU, Walpola BC, Yoon MH, 2013. Current status of heavy metal contamination in Asia’s rice lands. Rev Environ Sci Bio/Technol, 12(4):355-377.

[11]Aziz R, Rafiq MT, Li TQ, et al., 2015. Uptake of cadmium by rice grown on contaminated soils and its bioavailability/ toxicity in human cell lines (Caco-2/HL-7702). J Agric Food Chem, 63(13):3599-3608.

[12]Barabasz A, Wilkowska A, Tracz K, et al., 2013. Expression of HvHMA2 in tobacco modifies Zn-Fe-Cd homeostasis. J Plant Physiol, 170(13):1176-1186.

[13]Bashir K, Ishimaru Y, Nishizawa NK, 2012. Molecular mechanisms of zinc uptake and translocation in rice. Plant Soil, 361(1-2):189-201.

[14]CAC (Codex Alimentarius Commission), 2019. General Standard for Contaminants and Toxins in Food and Feed, Codex Standard 193-1995.

[15]Cao FB, Chen F, Sun HY, et al., 2014a. Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics, 15:611.

[16]Cao FB, Wang RF, Cheng WD, et al., 2014b. Genotypic and environmental variation in cadmium, chromium, lead and copper in rice and approaches for reducing the accumulation. Sci Total Environ, 496:275-281.

[17]Cao ZZ, Lin XY, Yang YJ, et al., 2019. Gene identification and transcriptome analysis of low cadmium accumulation rice mutant (lcd1) in response to cadmium stress using MutMap and RNA-seq. BMC Plant Biol, 19:250.

[18]Čásová K, Černý J, Száková J, et al., 2009. Cadmium balance in soils under different fertilization managements including sewage sludge application. Plant Soil Environ, 55(8):353-361.


[20]Chang AC, Page AL, Foster KW, et al., 1982. A comparison of cadmium and zinc accumulation by four cultivars of barley grown in sludge-amended soils. J Environ Qual, 11(2):409-412.

[21]Chen F, Wu FB, Dong J, et al., 2007a. Cadmium translocation and accumulation in developing barley grains. Planta, 227(1):223-232.

[22]Chen F, Dong J, Wang F, et al., 2007b. Identification of barley genotypes with low grain Cd accumulation and its interaction with four microelements. Chemosphere, 67(10):2082-2088.

[23]Chen HP, Yang XP, Wang P, et al., 2018. Dietary cadmium intake from rice and vegetables and potential health risk: a case study in Xiangtan, southern China. Sci Total Environ, 639:271-277.

[24]Chen JG, Zou WL, Meng LJ, et al., 2019. Advances in the uptake and transport mechanisms and QTLs mapping of cadmium in rice. Int J Mol Sci, 20(14):3417.

[25]Chen KL, Wang YP, Zhang R, et al., 2019. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol, 70:667-697.

[26]Ci DW, Jiang D, Li SS, et al., 2012. Identification of quantitative trait loci for cadmium tolerance and accumulation in wheat. Acta Physiol Plant, 34:191-202.

[27]Clarke JM, Leisle D, Kopytko GL, 1997. Inheritance of cadmium concentration in five durum wheat crosses. Crop Sci, 37(6):1722-1726.

[28]Clarke JM, Norvell WA, Clarke FR, et al., 2002. Concentration of cadmium and other elements in the grain of near-isogenic durum lines. Can J Plant Sci, 82(1):27-33.

[29]Clarke JM, McCaig TN, DePauw RM, et al., 2006. Registration of ‘Strongfield’ durum wheat. Crop Sci, 46(5):2306-2307.

[30]Clemens S, Ma JF, 2016. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol, 67:489-512.

[31]Clemens S, Aarts MGM, Thomine S, et al., 2013. Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci, 18(2):92-99.

[32]Cohen CK, Fox TC, Garvin DF, et al., 1998. The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol, 116(3):1063-1072.

[33]Cohen CK, Garvin DF, Kochian LV, 2004. Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta, 218(5):784-792.

[34]Connolly EL, Fett JP, Guerinot ML, 2002. Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell, 14(6):1347-1357.

[35]Curie C, Alonso JM, le Jean M, et al., 2000. Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J, 347:749-755.

[36]Dabeka RW, McKenzie AD, Lacroix GMA, 1987. Dietary intakes of lead, cadmium, arsenic and fluoride by Canadian adults: a 24-hour duplicate diet study. Food Add Contam, 4(1):89-101.

[37]Das N, Bhattacharya S, Bhattacharyya S, et al., 2017. Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol, 94(1-2):167-183.

[38]Du Y, Hu XF, Wu XH, et al., 2013. Affects of mining activities on Cd pollution to the paddy soils and rice grain in Hunan province, Central South China. Environ Monit Assess, 185(12):9843-9856.

[39]Eriksson JE, 1990. A field study on factors influencing Cd levels in soils and in grain of oats and winter wheat. Water Air Soil Poll, 53(1-2):69-81.

[40]Fahad S, Hussain S, Saud S, et al., 2015. Grain cadmium and zinc concentrations in maize influenced by genotypic variations and zinc fertilization. CLEAN-Soil Air Water, 43(10):1433-1440.

[41]Florijn PJ, van Beusichem ML, 1993a. Uptake and distribution of cadmium in maize inbred lines. Plant Soil, 150(1):25-32.

[42]Florijn PJ, van Beusichem ML, 1993b. Cadmium distribution in maize inbred lines: effects of pH and level of Cd supply. Plant Soil, 153(1):79-84.

[43]Grant CA, Clarke JM, Duguid S, et al., 2008. Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ, 390(2-3):301-310.

[44]Greger M, Löfstedt M, 2004. Comparison of uptake and distribution of cadmium in different cultivars of bread and durum wheat. Crop Sci, 44(2):501-507.

[45]Guttieri MJ, Seabourn BW, Liu CX, et al., 2015a. Distribution of cadmium, iron, and zinc in millstreams of hard winter wheat (Triticum aestivum L.). J Agric Food Chem, 63(49):10681-10688.

[46]Guttieri MJ, Baenziger PS, Frels K, et al., 2015b. Prospects for selecting wheat with increased zinc and decreased cadmium concentration in grain. Crop Sci, 55(4):1712-1728.

[47]Hao XH, Zeng M, Wang J, et al., 2018. A node-expressed transporter OsCCX2 is involved in grain cadmium accumulation of rice. Front Plant Sci, 9:476.

[48]He JY, Zhu C, Ren YF, et al., 2006. Genotypic variation in grain cadmium concentration of lowland rice. J Plant Nutr Soil Sci, 169(5):711-716.

[49]Hinesly TD, Alexander DE, Ziegler EL, et al., 1978. Zinc and Cd accumulation by corn inbreds grown on sludge amended soil. Agron J, 70(3):425-428.

[50]Hinesly TD, Alexander DE, Redborg KE, et al., 1982. Differential accumulations of cadmium and zinc by corn hybrids grown on soil amended with sewage sludge. Agron J, 74(3):469-474.

[51]Hirzel J, Retamal-Salgado J, Walter I, et al., 2017. Cadmium accumulation and distribution in plants of three durum wheat cultivars under different agricultural environments in Chile. J Soil Water Conserv, 72(1):77-88.

[52]Hirzel J, Retamal-Salgado J, Walter I, et al., 2018. Effect of soil cadmium concentration on three Chilean durum wheat cultivars in four environments. Arch Agron Soil Sci, 64(2):162-172.

[53]Hu DW, Sheng ZH, Li QL, et al., 2018. Identification of QTLs associated with cadmium concentration in rice grains. J Integr Agric, 17(7):1563-1573.

[54]Huang FL, Wei XJ, He JW, et al., 2018. Mapping of quantitative trait loci associated with concentrations of five trace metal elements in rice (Oryza sativa). Int J Agric Biol, 20(3):554-560.


[56]Huang YZ, Hu Y, Liu YX, 2009. Heavy metal accumulation in iron plaque and growth of rice plants upon exposure to single and combined contamination by copper, cadmium and lead. Acta Ecol Sin, 29(6):320-326.

[57]Ikeda M, Zhang ZW, Higashikawa K, et al., 1999. Background exposure of general women populations in Japan to cadmium in the environment and possible health effects. Toxicol Lett, 108(2-3):161-166.

[58]Ishikawa S, Ae N, Yano M, 2005. Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol, 168(2):345-350.

[59]Ishikawa S, Abe T, Kuramata M, et al., 2010. A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot, 61(3):923-934.

[60]Ishikawa S, Ishimaru Y, Igura M, et al., 2012. Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA, 109(47):19166-19171.

[61]Ishimaru Y, Takahashi R, Bashir K, et al., 2012. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep, 2:286.

[62]Järup L, Åkesson A, 2009. Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol, 238(3):201-208.

[63]Kashiwagi T, Shindoh K, Hirotsu N, et al., 2009. Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol, 9:8.

[64]Khan MA, Castro-Guerrero N, Mendoza-Cozatl DG, 2014. Moving toward a precise nutrition: preferential loading of seeds with essential nutrients over non-essential toxic elements. Front Plant Sci, 5:51.

[65]Knox RE, Pozniak CJ, Clarke FR, et al., 2009. Chromosomal location of the cadmium uptake gene (Cdu1) in durum wheat. Genome, 52(9):741-747.

[66]Kubo K, Kobayashi H, Fujita M, et al., 2016. Varietal differences in the absorption and partitioning of cadmium in common wheat (Triticum aestivum L.). Environ Exp Bot, 124:79-88.

[67]Lee S, An G, 2009. Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ, 32(4):408-416.

[68]Lee S, Kim YY, Lee Y, et al., 2007. Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol, 145(3):831-842.

[69]Li K, Yu HY, Li TX, et al., 2017. Cadmium accumulation characteristics of low-cadmium rice (Oryza sativa L.) line and F1 hybrids grown in cadmium-contaminated soils. Environ Sci Pollut Res, 24(21):17566-17576.

[70]Li S, Liu SM, Fu HW, et al., 2018. High-resolution melting-based TILLING of γ ray-induced mutations in rice. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 19(8):620-629.

[71]Liu JG, Zhu QS, Zhang ZJ, et al., 2005. Variations in cadmium accumulation among rice cultivars and types and the selection of cultivars for reducing cadmium in the diet. J Sci Food Agric, 85(1):147-153.

[72]Liu JG, Qian M, Cai GL, et al., 2007. Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater, 143(1-2):443-447.

[73]Liu SM, Jiang J, Liu Y, et al., 2019. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Sci, 26(2):88-97.

[74]Liu WQ, Pan XW, Li YC, et al., 2019. Identification of QTLs and validation of qCd-2 associated with grain cadmium concentrations in rice. Rice Sci, 26(1):42-49.

[75]Liu WX, Shang SH, Xue F, et al., 2015. Modulation of exogenous selenium in cadmium-induced changes in antioxidative metabolism, cadmium uptake, and photosynthetic performance in the 2 tobacco genotypes differing in cadmium tolerance. Environ Toxicol Chem, 2015, 34(1):92-99.

[76]Liu XS, Feng SJ, Zhang BQ, et al., 2019. OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol, 19:283.

[77]Lu CN, Zhang LX, Tang Z, et al., 2019. Producing cadmium-free Indica rice by overexpressing OsHMA3. Environ Int, 126: 619-626.

[78]Luo JS, Huang J, Zeng DL, et al., 2018. A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun, 9:645.

[79]McCouch SR, Wright MH, Tung CW, et al., 2016. Open access resources for genome-wide association mapping in rice. Nat Commun, 7:10532.

[80]Mills RF, Peaston KA, Runions J, et al., 2012. HvHMA2, a P1B-ATPase from barley, is highly conserved among cereals and functions in Zn and Cd transport. PLoS ONE, 7:e42640.

[81]Miyadate H, Adachi S, Hiraizumi A, et al., 2011. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol, 189(1):190-199.

[82]Murgia I, de Gara L, Grusak MA, 2013. Biofortification: how can we exploit plant science and biotechnology to reduce micronutrient deficiencies? Front Plant Sci, 4:429.

[83]Nakanishi H, Ogawa I, Ishimaru Y, et al., 2006. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr, 52(4):464-469.

[84]Nevo Y, Nelson N, 2006. The NRAMP family of metal-ion transporters. Biochim Biophys Acta, 1763(7):609-620.

[85]NHFPC (National Health and Family Planning Commission), 2017. National Safety Standard for Contaminants in Foods, GB2762-2017. National Standards of People’s Republic of China (in Chinese).

[86]Nicod J, Davies RW, Cai N, et al., 2016. Genome-wide association of multiple complex traits in outbred mice by ultra-low-coverage sequencing. Nat Genet, 48(8):912-918.

[87]Nordberg GF, 2009. Historical perspectives on cadmium toxicology. Toxicol Appl Pharmacol, 238(3):192-200.

[88]Oladzad-Abbasabadi A, Kumar A, Pirseyedi S, et al., 2018. Identification and validation of a new source of low grain cadmium accumulation in durum wheat. G3, 8(3):923-932.

[89]Oliver DP, Gartrell JW, Tiller KG, et al., 1995. Differential responses of Australian wheat cultivars to cadmium concentration in wheat grain. Aust J Agric Res, 46(5):873-886.

[90]Ovečka M, Takáč T, 2014. Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv, 32(1):73-86.

[91]Palmgren MG, Clemens S, Williams LE, et al., 2008. Zinc biofortification of cereals: problems and solutions. Trends Plant Sci, 13(9):464-473.

[92]Pedas P, Ytting CK, Fuglsang AT, et al., 2008. Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol, 148(1):455-466.

[93]Peng F, Wang C, Cheng YR, et al., 2018a. Cloning and characterization of TpNRAMP3, a metal transporter from Polish wheat (Triticum polonicum L.). Front Plant Sci, 9:1354.

[94]Peng F, Wang C, Zhu JS, et al., 2018b. Expression of TpNRAMP5, a metal transporter from polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta, 247(6):1395-1406.

[95]Penner GA, Bezte LJ, Leisle D, et al., 1995. Identification of RAPD markers linked to a gene governing cadmium uptake in durum wheat. Genome, 38(3):543-547.

[96]Perrier F, Yan B, Candaudap F, et al., 2016. Variability in grain cadmium concentration among durum wheat cultivars: impact of aboveground biomass partitioning. Plant Soil, 404(1-2):307-320.

[97]Pinson SRM, Tarpley L, Yan WG, et al., 2015. Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Sci, 55(1):294-311.

[98]Ramegowda Y, Venkategowda R, Jagadish P, et al., 2013. Expression of a rice Zn transporter, OsZIP1, increases Zn concentration in tobacco and finger millet transgenic plants. Plant Biotechnol Rep, 7(3):309-319.

[99]Randhawa HS, Asif M, Pozniak C, et al., 2013. Application of molecular markers to wheat breeding in Canada. Plant Breed, 132(5):458-471.

[100]Retamal-Salgado J, Hirzel J, Walter I, et al., 2017. Bioabsorption and bioaccumulation of cadmium in the straw and grain of maize (Zea mays L.) in growing soils contaminated with cadmium in different environment. Int J Environ Res Public Health, 14(11):1399.

[101]Ricachenevsky FK, Punshon T, Lee S, et al., 2018. Elemental profiling of rice FOX lines leads to characterization of a new Zn plasma membrane transporter, OsZIP7. Front Plant Sci, 9:865.

[102]Roberts TL, 2014. Cadmium and phosphorous fertilizers: the issues and the science. Procedia Eng, 83:52-59.

[103]Salsman E, Kumar A, AbuHammad W, et al., 2018. Development and validation of molecular markers for grain cadmium in durum wheat. Mol Breed, 38(3):28.

[104]Sasaki A, Yamaji N, Yokosho K, et al., 2012. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 24(5):2155-2167.

[105]Sasaki A, Yamaji N, Ma JF, 2014. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot, 65(20):6013-6021.

[106]Satarug S, Baker JR, Urbenjapol S, et al., 2003. A global perspective on cadmium pollution and toxicity in non-occupationally exposed population. Toxicol Lett, 137(1-2):65-83.

[107]Satarug S, Garrett SH, Sens MA, et al., 2009. Cadmium, environmental exposure, and health outcomes. Environ Health Persp, 118(2):182-190.

[108]Sato H, Shirasawa S, Maeda H, et al., 2011. Analysis of QTL for lowering cadmium concentration in rice grains from ‘LAC23’. Breed Sci, 61(2):196-200.

[109]Satoh-Nagasawa N, Mori M, Nakazawa N, et al., 2012. Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol, 53(1):213-224.

[110]Scofield GN, Hirose T, Aoki N, et al., 2007. Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot, 58(12):3155-3169.

[111]Sebastian A, Prasad MNV, 2014. Cadmium minimization in rice. A review. Agron Sustain Dev, 34:155-173.

[112]Shan QW, Wang YP, Li J, et al., 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc, 9(10):2395-2410.

[113]Shao JF, Xia JX, Yamaji N, et al., 2018. Effective reduction of cadmium accumulation in rice grain by expressing OsHMA3 under the control of the OsHMA2 promoter. J Exp Bot, 69(10):2743-2752.

[114]Shimo H, Ishimaru Y, An G, et al., 2011. Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot, 62(15):5727-5734.

[115]Song WE, Chen SB, Liu JF, et al., 2015. Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J Integr Agric, 14(9):1845-1854.

[116]Soric R, Loncaric Z, Kovacevic V, et al., 2009. A major gene for leaf cadmium accumulation in maize (Zea mays L.). The Proceedings of International Plant Nutrition Colloquium XVI, UC Davis: Department of Plant Sciences.

[117]Stolt JP, Sneller FEC, Bryngelsson T, et al., 2003. Phytochelatin and cadmium accumulation in wheat. Environ Exp Bot, 49(1):21-28.

[118]Sui FQ, Chang JD, Tang Z, et al., 2018. Nramp5 expression and functionality likely explain higher cadmium uptake in rice than in wheat and maize. Plant Soil, 433(1-2):377-389.

[119]Sun HY, Cao FB, Wang NB, et al., 2013. Differences in grain ultrastructure, phytochemical and proteomic profiles between the two contrasting grain Cd-accumulation barley genotypes. PLoS ONE, 2013, 8(11):e79158.

[120]Sun HY, Chen ZH, Chen F, et al., 2015. DNA microarray revealed and RNAi plants confirmed key genes conferring low Cd accumulation in barley grains. BMC Plant Biol, 15:259.

[121]Takahashi R, Ishimaru Y, Senoura T, et al., 2011a. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot, 62(14):4843-4850.

[122]Takahashi R, Ishimaru Y, Nakanishi H, et al., 2011b. Role of the iron transporter OsNRAMP1 in cadmium uptake and accumulation in rice. Plant Signal Behav, 6(11):1813-1816.

[123]Takahashi R, Ishimaru Y, Shimo H, et al., 2012. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ, 35(11):1948-1957.

[124]Tan JJ, Wang JW, Chai TY, et al., 2013. Functional analyses of TaHMA2, a P1B-type ATPase in wheat. Plant Biotechnol J, 11(4):420-431.

[125]Tan LT, Zhu YX, Fan T, et al., 2019. OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice. Biochem Biophys Res Commun, 512(1):112-118.

[126]Tang L, Mao BG, Li YK, et al., 2017. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep, 7:14438.

[127]Tezuka K, Miyadate H, Katou K, et al., 2010. A single recessive gene controls cadmium translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor Appl Genet, 120(6):1175-1182.

[128]Tsukahara T, Ezaki T, Moriguchi J, et al., 2003. Rice as the most influential source of cadmium intake among general Japanese population. Sci Total Environ, 305(1-3):41-51.

[129]Ueda Y, Frimpong F, Qi YT, et al., 2015. Genetic dissection of ozone tolerance in rice (Oryza sativa L.) by a genome-wide association study. J Exp Bot, 66(1):293-306.

[130]Ueno D, Koyama E, Kono I, et al., 2009a. Identification of a novel major quantitative trait locus controlling distribution of Cd between roots and shoots in rice. Plant Cell Physiol, 50(12):2223-2233.

[131]Ueno D, Kono I, Yokosho K, et al., 2009b. A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol, 182(3):644-653.

[132]Ueno D, Yamaji N, Kono I, et al., 2010. Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA, 107(38):16500-16505.

[133]Uraguchi S, Fujiwara T, 2013. Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol, 16(3):328-334.

[134]Uraguchi S, Kamiya T, Sakamoto T, et al., 2011. Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA, 108(52):20959-20964.

[135]Uraguchi S, Kamiya T, Clemens S, et al., 2014. Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiol Plant, 151(3):339-347.

[136]Uraguchi S, Tanaka N, Hofmann C, et al., 2017. Phytochelatin synthase has contrasting effects on cadmium and arsenic accumulation in rice grains. Plant Cell Physiol, 58(10):1730-1742.

[137]Vergine M, Aprile A, Sabella E, et al., 2017. Cadmium concentration in grains of durum wheat (Triticum turgidum L. subsp. durum). J Agric Food Chem, 65(30):6240-6246.

[138]Vert G, Barberon M, Zelazny E, et al., 2009. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta, 229(6):1171-1179.

[139]Wang XK, Gong X, Cao FB, et al., 2019. HvPAA1 encodes a P-Type ATPase, a novel gene for cadmium accumulation and tolerance in barley (Hordeum vulgare L.). Int J Mol Sci, 20(7):1732.

[140]Wang Y, Wang XL, Wang C, et al., 2017. Transcriptomic profiles reveal the interactions of Cd/Zn in dwarf Polish wheat (Triticum polonicum L.) roots. Front Physiol, 8:168.

[141]Waters BM, Sankaran RP, 2011. Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci, 180(4):562-574.

[142]White PJ, Broadley MR, 2005. Biofortifying crops with essential mineral elements. Trends Plant Sci, 10(12):586-593.

[143]WHO (World Health Organization), 2011. WHO Food Additives Series 64: Safety Evaluation of Certain Food Additives and Contaminants. Seventy-third Meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA), Geneva.

[144]Wiebe K, 2012. Molecular characterization of Cdu-b1, a major locus controlling cadmium accumulation in durum wheat (Triticum turgidum L. var durum) grain. MS Thesis, University of Saskatchewan, Saskatoon, Canada.

[145]Wiebe K, Harris NS, Faris JD, et al., 2010. Targeted mapping of Cdu1, a major locus regulating grain cadmium concentration in durum wheat (Triticum turgidum L. var durum). Theor Appl Genet, 121(6):1047-1058.

[146]Wu DZ, Sato K, Ma JF, 2015. Genome-wide association mapping of cadmium accumulation in different organs of barley. New Phytol, 208(3):817-829.

[147]Wu DZ, Yamaji N, Yamane M, et al., 2016. The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol, 172(3):1899-1910.

[148]Wu FB, Zhang G, 2002. Genotypic differences in effect of Cd on growth and mineral concentrations in barley seedlings. Bull Environ Contam Toxicol, 69(2):219-227.

[149]Wu FB, Wu HX, Zhang GP, et al., 2004. Differences in growth and yield in response to cadmium toxicity in cotton genotypes. J Plant Nutr Soil Sci, 167(1):85-90.

[150]Wu FB, Zhang GP, Dominy P, et al., 2007. Differences in yield components and kernel Cd accumulation in response to Cd toxicity in four barley genotypes. Chemosphere, 70(1):83-92.

[151]Xue DW, Chen MC, Zhang GP, 2009. Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica, 165(3):587.

[152]Yamaji N, Ma JF, 2014. The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci, 19(9):556-563.

[153]Yamaji N, Xia JX, Mitani-Ueno N, et al., 2013. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol, 162(2):927-939.

[154]Yan HL, Xu WX, Xie JY, et al., 2019. Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun, 10(1):2562.

[155]Yan JL, Wang PT, Wang P, et al., 2016. A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ, 39(9):1941-1954.

[156]Yan YF, Choi DH, Kim DS, et al., 2010. Genotypic variation of cadmium accumulation and distribution in rice. J Crop Sci Biotechnol, 13(2):69-73.

[157]Yan YF, Lestari P, Lee KJ, et al., 2013. Identification of quantitative trait loci for cadmium accumulation and distribution in rice (Oryza sativa). Genome, 56(4):227-232.

[158]Yang M, Zhang YY, Zhang LJ, et al., 2014. OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. J Exp Bot, 65(17):4849-4861.

[159]Yang YM, Nan ZR, Zhao ZJ, 2014. Bioaccumulation and translocation of cadmium in wheat (Triticum aestivum L.) and maize (Zea mays L.) from the polluted oasis soil of Northwestern China. Chem Spec Bioavailab, 26(1):43-51.

[160]Yousaf B, Liu GJ, Wang RW, et al., 2016. Bioavailability evaluation, uptake of heavy metals and potential health risks via dietary exposure in urban-industrial areas. Environ Sci Pollut Res, 23(22):22443-22453.

[161]Yu H, Wang JL, Fang W, et al., 2006. Cadmium accumulation in different rice cultivars and screening for pollution-safe cultivars of rice. Sci Total Environ, 370(2-3):302-309.

[162]Yuan LY, Yang SG, Liu BX, et al., 2012. Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep, 31(1):67-79.

[163]Yue JY, Wei XJ, Wang HZ, 2018. Cadmium tolerant and sensitive wheat lines: their differences in pollutant accumulation, cell damage, and autophagy. Biol Plant, 62(2):379-387.

[164]Zeng FR, Mao Y, Cheng WD, et al., 2008. Genotypic and environmental variation in chromium, cadmium and lead concentrations in rice. Environ Pollut, 153(2):309-314.

[165]Zhang L, Zhang L, Song FB, 2008. Cadmium uptake and distribution by different maize genotypes in maturing stage. Commun Soil Sci Plant Anal, 39(9-10):1517-1531.

[166]Zhang XH, Warburton ML, Setter T, et al., 2016. Genome-wide association studies of drought-related metabolic changes in maize using an enlarged SNP panel. Theor Appl Genet, 129(8):1449-1463.

[167]Zhang XQ, Zhang GP, Guo LB, et al., 2011. Identification of quantitative trait loci for Cd and Zn concentrations of brown rice grown in Cd-polluted soils. Euphytica, 180(2):173-179.

[168]Zhao JL, Yang W, Zhang SH, et al., 2018. Genome-wide association study and candidate gene analysis of rice cadmium accumulation in grain in a diverse rice collection. Rice, 11(1):61.

[169]Zhao XW, Luo LX, Cao YH, et al., 2018. Genome-wide association analysis and QTL mapping reveal the genetic control of cadmium accumulation in maize leaf. BMC Genomics, 19:91.

[170]Zhou Q, Shao GS, Zhang YX, et al., 2017. The difference of cadmium accumulation between the indica and japonica subspecies and the mechanism of it. Plant Growth Regul, 81(3):523-532. https://doi.org/10.1007/s10725-016-0229-0

[171]Zimmerl S, Lafferty J, Buerstmayr H, 2014. Assessing diversity in Triticum durum cultivars and breeding lines for high versus low cadmium content in seeds using the CAPS marker usw47. Plant Breed, 133(6):712-717.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE