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      Natural Variation at the FRD3 MATE Transporter Locus Reveals Cross-Talk between Fe Homeostasis and Zn Tolerance in Arabidopsis thaliana


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          Zinc (Zn) is essential for the optimal growth of plants but is toxic if present in excess, so Zn homeostasis needs to be finely tuned. Understanding Zn homeostasis mechanisms in plants will help in the development of innovative approaches for the phytoremediation of Zn-contaminated sites. In this study, Zn tolerance quantitative trait loci (QTL) were identified by analyzing differences in the Bay-0 and Shahdara accessions of Arabidopsis thaliana. Fine-scale mapping showed that a variant of the Fe homeostasis-related FERRIC REDUCTASE DEFECTIVE3 ( FRD3) gene, which encodes a multidrug and toxin efflux (MATE) transporter, is responsible for reduced Zn tolerance in A. thaliana. Allelic variation in FRD3 revealed which amino acids are necessary for FRD3 function. In addition, the results of allele-specific expression assays in F1 individuals provide evidence for the existence of at least one putative metal-responsive cis-regulatory element. Our results suggest that FRD3 works as a multimer and is involved in loading Zn into xylem. Cross-homeostasis between Fe and Zn therefore appears to be important for Zn tolerance in A. thaliana with FRD3 acting as an essential regulator.

          Author Summary

          Plants are adapted to soils in which the amounts of different nutrients vary widely, like Zn-deficient or Zn-contaminated soils. Exploring the molecular bases of plant adaptation to Zn-contaminated soils is important in determining strategies for phytoremediation. Here, we describe the mapping and characterization of a QTL for Zn tolerance in A. thaliana that underlies the natural variation of the root response to excess Zn. This physiological variation is controlled by different alleles of the AtFRD3 gene, which codes for a citrate transporter that uploads citrate into the xylem sap, hence playing a role in Fe homeostasis. In the Zn-sensitive accession Shahdara, the expression of AtFRD3 is drastically reduced and the protein encoded is unable to efflux citrate in vitro. Less Fe and Zn are found in Shahdara root exudates, and less Fe and Zn are translocated from root to shoot when Zn is in excess. We deduce that a fine-tuned Fe and Zn homeostasis is crucial for Zn tolerance in A. thaliana. Finally, as a range of alleles were identified, some rare, it was possible to define a sequence motif that is a putative metal-responsive cis-element and demonstrate that two amino acids are essential for the function of the FRD3 transporter.

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          Zinc in plants.

          Zinc (Zn) is an essential component of thousands of proteins in plants, although it is toxic in excess. In this review, the dominant fluxes of Zn in the soil-root-shoot continuum are described, including Zn inputs to soils, the plant availability of soluble Zn(2+) at the root surface, and plant uptake and accumulation of Zn. Knowledge of these fluxes can inform agronomic and genetic strategies to address the widespread problem of Zn-limited crop growth. Substantial within-species genetic variation in Zn composition is being used to alleviate human dietary Zn deficiencies through biofortification. Intriguingly, a meta-analysis of data from an extensive literature survey indicates that a small proportion of the genetic variation in shoot Zn concentration can be attributed to evolutionary processes whose effects manifest above the family level. Remarkable insights into the evolutionary potential of plants to respond to elevated soil Zn have recently been made through detailed anatomical, physiological, chemical, genetic and molecular characterizations of the brassicaceous Zn hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri.
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            Evolutionary changes in cis and trans gene regulation.

            Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.
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              Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants.

              Nitrate is both a nitrogen source for higher plants and a signal molecule regulating their development. In Arabidopsis, the NRT1.1 nitrate transporter is crucial for nitrate signaling governing root growth, and has been proposed to act as a nitrate sensor. However, the sensing mechanism is unknown. Herein we show that NRT1.1 not only transports nitrate but also facilitates uptake of the phytohormone auxin. Moreover, nitrate inhibits NRT1.1-dependent auxin uptake, suggesting that transduction of nitrate signal by NRT1.1 is associated with a modification of auxin transport. Among other effects, auxin stimulates lateral root development. Mutation of NRT1.1 enhances both auxin accumulation in lateral roots and growth of these roots at low, but not high, nitrate concentration. Thus, we propose that NRT1.1 represses lateral root growth at low nitrate availability by promoting basipetal auxin transport out of these roots. This defines a mechanism connecting nutrient and hormone signaling during organ development. Copyright 2010 Elsevier Inc. All rights reserved.

                Author and article information

                Role: Editor
                PLoS Genet
                PLoS Genet
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                December 2012
                December 2012
                6 December 2012
                : 8
                : 12
                [1 ]CNRS-INRA-MontpellierSupAgro-UM2, UMR Biochimie et Physiologie Moléculaire des Plantes, Montpellier, France
                [2 ]INRA, UMR1318, Institut Jean-Pierre Bourgin, Versailles, France
                University of Lausanne, Switzerland
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CP BL OL PB OR. Performed the experiments: CP SL CL CC CF BL MF OR. Analyzed the data: CP SL CL OL PB OR. Contributed reagents/materials/analysis tools: CF OL. Wrote the paper: OL PB OR.


                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 10
                CP was supported by a post-doctoral fellowship from the French National Institute for Agricultural Research-INRA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Research Article
                Plant Science
                Plant Genetics
                Plant Physiology



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