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      Association Study Reveals Genetic Loci Responsible for Arsenic, Cadmium and Lead Accumulation in Rice Grain in Contaminated Farmlands

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          Abstract

          Accumulation of toxic heavy metals and metalloids (THMMs) in crop grain remarkably affects food safety and human health. Reducing the content of THMMs in grain requires the identification and manipulation of the genes regulating their accumulation. This study aimed to determine the genetic variations affecting grain THMM accumulation in rice by using association mapping. We used 276 accessions with 416 K single nucleotide polymorphisms (SNPs) and performed genome-wide association analysis of grain THMM concentrations in rice grown in heavily multi-contaminated farmlands. We detected 22, 17, and 21 quantitative trait loci (QTLs) for grain arsenic, cadmium, and lead concentrations, respectively. Both inter- and intra-subpopulation variants accounted for these QTLs. Most QTLs contained no known THMM-related genes and represented unidentified novel genes. We examined the candidate genes in qGAS1, a QTL for grain arsenic concentration with the best P-value detected for the entire population. We speculated that a transport protein of the multidrug and toxin extrusion family could be the candidate gene for this QTL. Our study suggested that the genetic regulation of grain THMM accumulation is very complex and largely unknown. The QTLs and SNPs identified in this study might help in the identification of new genes regulating THMM accumulation and aid in marker-assisted breeding of rice with low grain THMM content.

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          Most cited references 56

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          Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter.

          Despite dramatic declines in children's blood lead concentrations and a lowering of the Centers for Disease Control and Prevention's level of concern to 10 microg per deciliter (0.483 micromol per liter), little is known about children's neurobehavioral functioning at lead concentrations below this level. We measured blood lead concentrations in 172 children at 6, 12, 18, 24, 36, 48, and 60 months of age and administered the Stanford-Binet Intelligence Scale at the ages of 3 and 5 years. The relation between IQ and blood lead concentration was estimated with the use of linear and nonlinear mixed models, with adjustment for maternal IQ, quality of the home environment, and other potential confounders. The blood lead concentration was inversely and significantly associated with IQ. In the linear model, each increase of 10 microg per deciliter in the lifetime average blood lead concentration was associated with a 4.6-point decrease in IQ (P=0.004), whereas for the subsample of 101 children whose maximal lead concentrations remained below 10 microg per deciliter, the change in IQ associated with a given change in lead concentration was greater. When estimated in a nonlinear model with the full sample, IQ declined by 7.4 points as lifetime average blood lead concentrations increased from 1 to 10 microg per deciliter. Blood lead concentrations, even those below 10 microg per deciliter, are inversely associated with children's IQ scores at three and five years of age, and associated declines in IQ are greater at these concentrations than at higher concentrations. These findings suggest that more U.S. children may be adversely affected by environmental lead than previously estimated. Copyright 2003 Massachusetts Medical Society
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            Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice.

            Paddy rice (Oryza sativa) is able to accumulate high concentrations of Mn without showing toxicity; however, the molecular mechanisms underlying Mn uptake are unknown. Here, we report that a member of the Nramp (for the Natural Resistance-Associated Macrophage Protein) family, Nramp5, is involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice. Nramp5 was constitutively expressed in the roots and encodes a plasma membrane-localized protein. Nramp5 was polarly localized at the distal side of both exodermis and endodermis cells. Knockout of Nramp5 resulted in a significant reduction in growth and grain yield, especially when grown at low Mn concentrations. This growth reduction could be partially rescued by supplying high concentrations of Mn but not by the addition of Fe. Mineral analysis showed that the concentration of Mn and Cd in both the roots and shoots was lower in the knockout line than in wild-type rice. A short-term uptake experiment revealed that the knockout line lost the ability to take up Mn and Cd. Taken together, Nramp5 is a major transporter of Mn and Cd and is responsible for the transport of Mn and Cd from the external solution to root cells.
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              Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice.

              A genome-wide association study (GWAS) can be a powerful tool for the identification of genes associated with agronomic traits in crop species, but it is often hindered by population structure and the large extent of linkage disequilibrium. In this study, we identified agronomically important genes in rice using GWAS based on whole-genome sequencing, followed by the screening of candidate genes based on the estimated effect of nucleotide polymorphisms. Using this approach, we identified four new genes associated with agronomic traits. Some genes were undetectable by standard SNP analysis, but we detected them using gene-based association analysis. This study provides fundamental insights relevant to the rapid identification of genes associated with agronomic traits using GWAS and will accelerate future efforts aimed at crop improvement.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                05 February 2019
                2019
                : 10
                Affiliations
                1College of Materials and Environmental Engineering, Hangzhou Dianzi University , Hangzhou, China
                2Laboratory of Photosynthesis and Environmental Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences , Shanghai, China
                3Key Laboratory for Water Pollution Control and Environmental Safety of Zhejiang Province, Zhejiang University , Hangzhou, China
                4State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Agriculture, Nanjing Agricultural University , Nanjing, China
                5China National Rice Research Institute , Hangzhou, China
                6Bio-Med Big Data Center, CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences , Shanghai, China
                Author notes

                Edited by: Luigi Cattivelli, The Council for Agricultural Research and Economics, Italy

                Reviewed by: Gian Attilio Sacchi, University of Milan, Italy; Giampiero Valè, Cereal Research Centre, CRA-CER, Italy

                *Correspondence: Sheng Teng, steng@ 123456sibs.ac.cn

                These authors have contributed equally to this work

                This article was submitted to Plant Breeding, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.00061
                6370710
                Copyright © 2019 Liu, Chen, Chen, Zheng, Peng, Shi, Qin, Xu and Teng.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 9, Tables: 6, Equations: 0, References: 70, Pages: 16, Words: 0
                Categories
                Plant Science
                Original Research

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