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      A single‐population GWAS identified AtMATE expression level polymorphism caused by promoter variants is associated with variation in aluminum tolerance in a local Arabidopsis population

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          Abstract

          Organic acids (OA) are released from roots in response to aluminum (Al), conferring an Al tolerance to plants that is regulated by OA transporters such as ALMT (Al‐activated malate transporter) and multi‐drug and toxic compound extrusion (MATE). We have previously reported that the expression level polymorphism (ELP) of AtALMT1 is strongly associated with variation in Al tolerance among natural accessions of Arabidopsis. However, although AtMATE is also expressed following Al exposure and contributes to Al tolerance, whether AtMATE contributes to the variation of Al tolerance and the molecular mechanisms of ELP remains unclear. Here, we dissected the natural variation in AtMATE expression level in response to Al at the root using diverse natural accessions of Arabidopsis. Phylogenetic analysis revealed that more than half of accessions belonging to the Central Asia (CA) population show markedly low AtMATE expression levels, while the majority of European populations show high expression levels. The accessions of the CA population with low AtMATE expression also show significantly weakened Al tolerance. A single‐population genome‐wide association study (GWAS) of AtMATE expression in the CA population identified a retrotransposon insertion in the AtMATE promoter region associated with low gene expression levels. This may affect the transcriptional regulation of AtMATE by disrupting the effect of a cis‐regulatory element located upstream of the insertion site, which includes AtSTOP1 (sensitive to proton rhizotoxicity 1) transcription factor‐binding sites revealed by chromatin immunoprecipitation‐qPCR analysis. Furthermore, the GWAS performed without the accessions expressing low levels of AtMATE, excluding the effect of AtMATE promoter polymorphism, identified several candidate genes potentially associated with AtMATE expression.

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          Whole-genome sequencing of multiple Arabidopsis thaliana populations.

          The plant Arabidopsis thaliana occurs naturally in many different habitats throughout Eurasia. As a foundation for identifying genetic variation contributing to adaptation to diverse environments, a 1001 Genomes Project to sequence geographically diverse A. thaliana strains has been initiated. Here we present the first phase of this project, based on population-scale sequencing of 80 strains drawn from eight regions throughout the species' native range. We describe the majority of common small-scale polymorphisms as well as many larger insertions and deletions in the A. thaliana pan-genome, their effects on gene function, and the patterns of local and global linkage among these variants. The action of processes other than spontaneous mutation is identified by comparing the spectrum of mutations that have accumulated since A. thaliana diverged from its closest relative 10 million years ago with the spectrum observed in the laboratory. Recent species-wide selective sweeps are rare, and potentially deleterious mutations are more common in marginal populations.
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            Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension.

            Gene splicing by overlap extension is a new approach for recombining DNA molecules at precise junctions irrespective of nucleotide sequences at the recombination site and without the use of restriction endonucleases or ligase. Fragments from the genes that are to be recombined are generated in separate polymerase chain reactions (PCRs). The primers are designed so that the ends of the products contain complementary sequences. When these PCR products are mixed, denatured, and reannealed, the strands having the matching sequences at their 3' ends overlap and act as primers for each other. Extension of this overlap by DNA polymerase produces a molecule in which the original sequences are 'spliced' together. This technique is used to construct a gene encoding a mosaic fusion protein comprised of parts of two different class-I major histocompatibility genes. This simple and widely applicable approach has significant advantages over standard recombinant DNA techniques.
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              A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.

              Crop yields are significantly reduced by aluminum toxicity on highly acidic soils, which comprise up to 50% of the world's arable land. Candidate aluminum tolerance proteins include organic acid efflux transporters, with the organic acids forming non-toxic complexes with rhizosphere aluminum. In this study, we used positional cloning to identify the gene encoding a member of the multidrug and toxic compound extrusion (MATE) family, an aluminum-activated citrate transporter, as responsible for the major sorghum (Sorghum bicolor) aluminum tolerance locus, Alt(SB). Polymorphisms in regulatory regions of Alt(SB) are likely to contribute to large allelic effects, acting to increase Alt(SB) expression in the root apex of tolerant genotypes. Furthermore, aluminum-inducible Alt(SB) expression is associated with induction of aluminum tolerance via enhanced root citrate exudation. These findings will allow us to identify superior Alt(SB) haplotypes that can be incorporated via molecular breeding and biotechnology into acid soil breeding programs, thus helping to increase crop yields in developing countries where acidic soils predominate.
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                Author and article information

                Contributors
                k_yuriko@gifu-u.ac.jp
                Journal
                Plant Direct
                Plant Direct
                10.1002/(ISSN)2475-4455
                PLD3
                Plant Direct
                John Wiley and Sons Inc. (Hoboken )
                2475-4455
                12 August 2020
                August 2020
                : 4
                : 8 ( doiID: 10.1002/pld3.v4.8 )
                : e00250
                Affiliations
                [ 1 ] Faculty of Applied Biological Sciences Gifu University Gifu Gifu Japan
                [ 2 ] Global Institute for Food Security University of Saskatchewan Saskatoon SK Canada
                [ 3 ] Experimental Plant Division RIKEN BioResource Research Center Tsukuba Ibaraki Japan
                Author notes
                [*] [* ] Correspondence

                Yuriko Kobayashi, Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu, Gifu, Japan.

                Email: k_yuriko@ 123456gifu-u.ac.jp

                Article
                PLD3250
                10.1002/pld3.250
                7419912
                32793853
                0eeab208-bfc2-4fe1-adf1-784105e4d2b2
                © 2020 The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 March 2020
                : 10 July 2020
                : 13 July 2020
                Page count
                Figures: 7, Tables: 1, Pages: 14, Words: 9716
                Funding
                Funded by: JSPS KAKENHI
                Award ID: 18J11757
                Award ID: 19K05753
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                August 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.6 mode:remove_FC converted:12.08.2020

                al tolerance,gwas,mate,natural variation,stop1,transposon
                al tolerance, gwas, mate, natural variation, stop1, transposon

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