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      Association and Linkage Analysis of Aluminum Tolerance Genes in Maize

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          Abstract

          Background

          Aluminum (Al) toxicity is a major worldwide constraint to crop productivity on acidic soils. Al becomes soluble at low pH, inhibiting root growth and severely reducing yields. Maize is an important staple food and commodity crop in acidic soil regions, especially in South America and Africa where these soils are very common. Al exclusion and intracellular tolerance have been suggested as two important mechanisms for Al tolerance in maize, but little is known about the underlying genetics.

          Methodology

          An association panel of 282 diverse maize inbred lines and three F 2 linkage populations with approximately 200 individuals each were used to study genetic variation in this complex trait. Al tolerance was measured as net root growth in nutrient solution under Al stress, which exhibited a wide range of variation between lines. Comparative and physiological genomics-based approaches were used to select 21 candidate genes for evaluation by association analysis.

          Conclusions

          Six candidate genes had significant results from association analysis, but only four were confirmed by linkage analysis as putatively contributing to Al tolerance: Zea mays Alt SB like ( ZmASL), Zea mays aluminum-activated malate transporter2 ( ALMT2), S-adenosyl-L-homocysteinase (SAHH), and Malic Enzyme ( ME). These four candidate genes are high priority subjects for follow-up biochemical and physiological studies on the mechanisms of Al tolerance in maize. Immediately, elite haplotype-specific molecular markers can be developed for these four genes and used for efficient marker-assisted selection of superior alleles in Al tolerance maize breeding programs.

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          Most cited references23

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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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            Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification.

            Dietary vitamin A deficiency causes eye disease in 40 million children each year and places 140 to 250 million at risk for health disorders. Many children in sub-Saharan Africa subsist on maize-based diets. Maize displays considerable natural variation for carotenoid composition, including vitamin A precursors alpha-carotene, beta-carotene, and beta-cryptoxanthin. Through association analysis, linkage mapping, expression analysis, and mutagenesis, we show that variation at the lycopene epsilon cyclase (lcyE) locus alters flux down alpha-carotene versus beta-carotene branches of the carotenoid pathway. Four natural lcyE polymorphisms explained 58% of the variation in these two branches and a threefold difference in provitamin A compounds. Selection of favorable lcyE alleles with inexpensive molecular markers will now enable developing-country breeders to more effectively produce maize grain with higher provitamin A levels.
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              Aluminum Toxicity and Tolerance in Plants.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                1 April 2010
                : 5
                : 4
                Affiliations
                [1 ]United States Department of Agriculture-Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, New York, United States of America
                [2 ]Cornell University, Department of Plant Breeding and Genetics, Ithaca, New York, United States of America
                [3 ]Institute for Genomic Diversity, Cornell University, Ithaca, New York, United States of America
                [4 ]University of Florida, School of Forest Resources and Conservation, Gainesville, Florida, United States of America
                [5 ]Cornell University, Department of Plant Biology, Ithaca, New York, United States of America
                East Carolina University, United States of America
                Author notes

                Conceived and designed the experiments: AMK MK LVK EB OH. Performed the experiments: AMK MK. Analyzed the data: AMK MK EB OH. Wrote the paper: AMK LVK EB OH.

                Article
                09-PONE-RA-14278R1
                10.1371/journal.pone.0009958
                2848604
                20376361
                ce4c1085-5e00-434c-bce9-d93548516c13
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                Page count
                Pages: 11
                Categories
                Research Article
                Genetics and Genomics/Complex Traits
                Plant Biology/Agricultural Biotechnology
                Plant Biology/Plant Genetics and Gene Expression
                Plant Biology/Plant Genomes and Evolution
                Plant Biology/Plant-Environment Interactions

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                Uncategorized

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