Abstract
Excess trace metals may cause damage to human health due to the consumption of food grain grown in contaminated soils. This study was designed to understand the genetic mechanisms of copper (Cu) and zinc (Zn) accumulation in wheat grain under stressed environments. The differences of Cu/Zn contents in the grain among 246 wheat varieties were analyzed, and the wheat varieties with low or high accumulation of Cu and Zn in the safe range were also screened out. The accumulation of Cu and Zn in grains of “Chushanbao” was lowest, which could be used as a novel germplasm for wheat breeding under heavy metal stress. We found that Cu contents of wheat grain were significantly and positively correlated with Zn. The quantitative trait loci (QTLs) for grain Cu content (GCuC) and grain Zn content (GZnC) were detected by genome-wide association study (GWAS). Twenty-three loci affecting GCuC were identified on chromosomes 1A, 1D, 2A, 2B, 2D, 3A, 3B, 3D, 4A, 4B 4D, 5A, 6D, 7A, and 7B, explaining 2.6–5.8% of the phenotypic variation. Sixteen loci associated with the GZnC on 11 different chromosomes 1B, 2B, 2D, 3A, 3D, 4A, 4B, 5A, 5D, 6B, and 7D were detected, which could explain 2.7~6.6% of phenotypic variance. We also determined five associated loci on chromosomes 2B, 2D, 3A, 4B, and 5A were in pleiotropic regions affecting both GCuC and GZnC. This study would help in better understanding the molecular basis of Cu/Zn accumulation in wheat grain, and the associated markers may be useful for marker-assisted selection (MAS) breeding program.
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References
Agrawal V, Sharma K (2006) Phytotoxic effects of Cu, Zn, Cd and Pb on in vitro regeneration and concomitant protein changes in Holarrhena antidysenterica. Biol Plant 50:307–310
Akdas S, Turan B, Durak A, Ayral PA, Yazihan N (2020) The relationship between metabolic syndrome development and tissue trace elements status and inflammatory markers. Bio Trace Elem Res 198:16–24. https://doi.org/10.1007/s12011-020-02046-6
Bálint AF, Kováca G, Börner A, Galiba G, Sutka J (2003) Substitution analysis of seedling stage copper tolerance in wheat. Acta Agronomica Hungarica 51:397–404
Bálint AF, Röder MS, Hell R, Galiba G, Börner A (2007) Mapping of QTLs affecting copper tolerance and the Cu, Fe, Mn and Zn contents in the shoots of wheat seedlings. Biol Plantarum 51:129–134
Bradbury PJ, Zhang Z, Kroon DE, Cassteven TM, Ramdoss Y, Bucker ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Bruns HA, Ebelhar MW (2006) Nutrient uptake of maize affected by nitrogen and potassium fertility in a humid subtropical environment. Commun Soil Sci Plant Anal 37:275–293
Chandra R, Yadav SY, Adav S (2017) Phytoextraction potential of heavy metals by native wetland plants growing on chlorolign in containing sludge of pulp and paper industry. Ecol Eng 98:134–145
Chen YH, Mao Y, He SB, Guo P, Xu K (2007) Heat stress increases the efficiency of EDTA in phytoextraction of heavy metals. Chemosphere 67:1511–1517
Dalgaard MM, Pedas P, Schiller M, Vincze E, Mills RF, Borg S, Moller A, Schjoerring JK, Williams LE, Baekgaad L, Holm PB, Palmgren MG (2012) Barley HvHMA1 is a heavy metal pump involved in mobilizing organellar Zn and Cu and plays a role in metal loading into grains. Plos One 7:e49027
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Ganeva G, Landjeva S, Merakchijska M (2003) Effects of chromosome substitutions on copper toxicity tolerance in wheat seedlings. Biol Plantarum 47:621–623
Hakanson L (1980) An ecological risk index for aquatic pollution control toxicity tolerance in wheat seedling. Water Res 14:975–1001
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266
Hao CY, Dong YC, Wang LF, You GX, Zhang HN, Ge HM, Jia JZ, Zhang XY (2008) Genetic diversity and construction of core collection in Chinese wheat genetic resources. Chinese Sci Bull 53:1518–1526
Hao CY, Wang LF, Ge HM, Dong YC, Zhang XY (2011) Genetic diversity and linkage disequilibrium in Chinese bread wheat (Triticum aestivum L.) revealed by SSR markers. PloS One 6:e17279
Hao Y, Velu G, Peña RJ, Singh S, Singh RP (2014) Genetic loci associated with high grain zinc concentration and pleiotropic effect on kernel weight in wheat (Triticum aestivum L.). Mol Breeding 34:1893–1902
Huang ML, Zhou SL, Sun B, Zhao QG (2008) Heavy metals in wheat grain: assessment of potential health risk for inhabitants in Kushan, China. Sci Total Environ 405:54–61
Huang SS, Tu J, Liu HY, Hua M, Liao QL, Feng JS, Weng ZH, Huang GM (2009) Multivariate analysis of trace element concentrations in atmospheric deposition in the Yangtze River Delta, East China. Atmos Environ 43:5781–5790
Jaradat AA (2017) Phenotypic and ionome profiling of Triticum aestivum 9 Aegilops tauschii introgression lines. Crop Sci 57:1916–1934
Karaman MR, Tuşat E, Er F, Turan M, Dizman M (2013) Assessment of resistance of wheat genotypes (T. aestivum and T. durum) to copper toxicity. J Food Agric Environ 11:580–583
Khan K, Lu YL, Khan H, Ishtiaq M, Khan S, Waqas M, Wei L, Wang TY (2013a) Heavy metals in agricultural soils and crops and their health risks in Swat District, northern Pakistan. Food Chem Toxicol 58:449–458
Khan ZI, Ahmad K, Ashraf M, Akram NA, Rizwan Y, Shaheen M, Arshad F (2013b) Assessment of potential toxicological risk for public health of heavy metals in wheat crop irrigated with wastewater: a case study in Sargodha, Pakistan. Asian J Chem 25:9704–9706
Kumar R, Mehrotra NK, Nautiyal BD, Kumar P, Singh PK (2009) Effect of copper on growth, yield and concentration of Fe, Mn, Zn and Cu in wheat plants (Triticum aestivum L.). J Environ Biol 30:485–488
Kung WJ, Shih CT, Lee CH, Lin CC (2018) The divalent elements changes in early stages of chronic kidney disease. Biol Trace Elem Res 185:30–35
Lee S, Jeon US, Lee SJ, Kim YK, Persson DP, Husted S, Schjorring JK, Kakei Y, Masuda H, Nishizawa NK, An G (2009) Iron fortification of rice seeds through activation of the nicotianamine synthase gene. P Natl Acad Sci USA 106:22014–22019
Li H, Fan R, Li L, Wei B, Li G, Gu L, Wang XP, Zhang XQ (2014) Identification and characterization of a novel copper transporter gene family TaCT1 in common wheat. Plant Cell Environ 37:1561–1573
Lysenko EA, Klaus AA, Kartashov AV, Kusnetsov VV (2020) Specificity of Cd, Cu, and Fe effects on barley growth, metal contents in leaves and chloroplasts, and activities of photosystem I and photosystem II. Plant Physiol Bioch 147:191–204
Ma BL, Zheng ZM (2018) Nutrient uptake of iron, zinc, magnesium, and copper in transgenic maize (Zea mays) as affected by rotation systems and N application rates. Nutr Cycl Agroecosyst 112:27–43
Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: a review with special reference to phytoremediation. Int J Environ Sci Technol 11:843–872
Manyowa NM, Miller TE (1991) The genetic of tolerance to high mineral concentrations in the tribe Triticeae – a review and update. Euphytica 57:175–185
Meena K, Sarita S (2019) Bioremediation options for heavy metal pollution. J H Pollut 9(24):191203
Menguer P, Vincent T, Miller AJ, Brown JKM, Vincze E, Borg S, Holm PB, Sanders D, Podar D (2017) Improving zinc accumulation in barley endosperm using HvMTP1, a transition metal transporter. Plant Biotechnol J 16:63–71
Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8:107–122
Muhammad S, Shah MT, Khan S (2011) Health risk assessment of heavy metals and their source apportionment in drinking water of Kohistan region, northern Pakistan. Microchem J 98:334–343
Nicholls AM, Mal TK (2003) Effects of lead and copper exposure on growth of an invasive weed, Lythrum salicaria L. (Purple Loosestrife). Ohio J Sci 103:129–133
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959
Sarwar N, Saifullah MSS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of plant nutrients in minimizing cadmium accumulation by plant. J Sci Food Agric 90:925–937
Sarwar N, Imran M, Shaheen MR, Ishaq W, Kamran A, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721
Sharma S, Kaur G, Kumar A, Meena V, Ram H, Kaur J, Pandey AK (2020) Gene expression pattern of vacuolar-iron transporter-like (VTL) genes in hexaploid wheat during metal stress. Plants-Basel 9(2):229
Shi RL, Li HW, Tong YP, Jing RL, Zhang FS, Zou CQ (2008) Identification of quantitative trait locus of zinc and phosphorus density in wheat (Triticum aestivum L.) grain. Plant Soil 306:95–104
Singh S, Aggarwal PK (2005) Effect of heavy metal fertilization on growth, yield and metal distribution in wheat. Indian J Plant Physiol 10:302–305
Singh RP, Jha PN (2018) Priming with ACC-utilizing bacterium attenuated copper toxicity, improved oxidative stress tolerance, and increased phytoextraction capacity in wheat. Environ Sci Pollut R 25(33):33755–33767
Tani FH, Barrington S (2005) Zinc and copper uptake by plants under two transpiration rates. Part I. Wheat (Triticum aestivum L.). Environ Pollut 138(3):538–547
Tauris B, Borg S, Gregersen PL, Holm PB (2009) A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J Exp Bot 60:1333–1347
Wang H, Zhong G, Shi G, Pan F (2010) Toxicity of Cu, Pb, and Zn on seed germination and young seedlings of wheat (Triticum aestivum L.). CCTA 346:231–240
Wang C, Yang ZF, Yuan XY, Browne P, Chen LX, Ji JF (2013) The influences of soil properties on Cu and Zn availability in soil and their transfer to wheat (Triticum aestivum L) in the Yangtze River delta region, China. Geoderma 193:131–139
Wang JJ, Yu N, Mu GM, Shinwari KI, Shen ZG, Zheng LQ (2017a) Screening for Cd-safe cultivars of Chinese cabbage and a preliminary study on the mechanisms of Cd Accumulation. Inter J Env Res Pub Heal 14:395
Wang XD, Ji DX, Chen XL, Ma YB, Yang JX, Ma JX, Li XX (2017b) Extended biotic ligand model for predicting combined Cu-Zn toxicity to wheat (Triticum aestivum L.): incorporating the effects of concentration ratio, major cations and pH. Environ Pollut 230:210–217
Wang WH, Luo XG, Zhe W, Yu Z, Wu FQ, Li ZX (2018) Heavy metal and metalloid contamination assessments of soil around an abandoned uranium tailings pond and the contaminations’ spatial distribution and variability. Inter J Env Res Pub Heal 15(11):2401
Wang FF, Guan QY, Tian J, Lin JK, Yang YY, Yang LQ, Pan NH (2020) Contamination characteristics, source apportionment, and health risk assessment of heavy metals in agricultural soil in the Hexi Corridor. Catena 191:104573
Wu C, Xue S (2018) Element Case Studies: Manganese. Agromining: farming for metals: Extracting unconventional resources using plants. Miner Resour Rev pp:263–273
Wu F, Liu YL, Xia Y, Shen ZG, Chen YH (2011) Copper contamination of soils and vegetables in the vicinity of Jiuhuashan copper mine, China. Environ Earth Sci 64:761–769
Yang QQ, Li ZY, Lu XN, Duan QN, Huang L, Bi J (2018) A review of soil heavy metal pollution from industrial and agricultural regions in China: pollution and risk assessment. Sci Total Environ 642:690–700
Zhang K, Wang JB, Yang ZY, Xin GR, Yuan JG, Xin JL, Huang C (2013) Genotype variations in accumulation of cadmium and lead in celery (Apium graveolens L.) and screening for low Cd and Pb accumulative cultivars. Front Env Sci Eng 7:85–96
Zhou ZF, Shi X, Zhao GQ, Mao M, Lbba MI, Wang YH, Li WX, Yang P, Wu ZQ, Lei ZS, Wang JS (2020) Identification of novel genomic regions and superior alleles associated with Zn accumulation in wheat using a genome-wide association analysis method. Int J Mol Sci 21:1928
Funding
This research was financially supported by the National Key Research and Development Program (2016YFD08007003), National Natural Science Foundation of China (31871619, 31901180, 41571307), China Postdoctoral Science Foundation (2019M651845), Special Fund Project of Fundamental Scientific Research Funds for Central Universities of Nanjing Agricultural University (KYQN202061), and Jiangsu Agriculture Science and Technology Innovation Fund (JASTIF) (CX (17) 3004) in China.
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Ying Liu and Yaru Chen analyzed the soil physical, chemical properties, and metal element contents in plant and soil samples. Yang Yang finished the part of genotyping. Qiaofeng Zhang found and arranged the pollution assessment standard. Bisheng Fu finished the statistical analysis. Jin Cai and Wei Guo planted and harvested wheat. Liang Shi and Jizhong Wu were the two major contributors in writing the manuscript. Yahua Chen provided the experimental programs and ideas. All the authors read and approved the final manuscript.
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Liu, Y., Chen, Y., Yang, Y. et al. A thorough screening based on QTLs controlling zinc and copper accumulation in the grain of different wheat genotypes. Environ Sci Pollut Res 28, 15043–15054 (2021). https://doi.org/10.1007/s11356-020-11690-3
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DOI: https://doi.org/10.1007/s11356-020-11690-3