Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, [2003]-

Genome-Wide Association Study*; Arabidopsis/*enzymology ; Arabidopsis/*genetics ; Arabidopsis Proteins/*metabolism ; Arsenate Reductases/*metabolism ; Arsenic/*metabolism; Amino Acid Sequence ; Arabidopsis Proteins/genetics ; Arsenate Reductases/genetics ; Epistasis, Genetic ; Genes, Plant ; Genetic Loci ; Models, Biological ; Molecular Sequence Data ; Plant Leaves/metabolism ; Plant Roots/metabolism ; Plant Shoots/metabolism ; Reproducibility of Results ; Sequence Analysis, Protein

Inorganic arsenic is a carcinogen, and its ingestion through foods such as rice presents a significant risk to human health. Plants chemically reduce arsenate to arsenite. Using genome-wide association (GWA) mapping of loci controlling natural variation in arsenic accumulation in Arabidopsis thaliana allowed us to identify the arsenate reductase required for this reduction, which we named High Arsenic Content 1 (HAC1). Complementation verified the identity of HAC1, and expression in Escherichia coli lacking a functional arsenate reductase confirmed the arsenate reductase activity of HAC1. The HAC1 protein accumulates in the epidermis, the outer cell layer of the root, and also in the pericycle cells surrounding the central vascular tissue. Plants lacking HAC1 lose their ability to efflux arsenite from roots, leading to both increased transport of arsenic into the central vascular tissue and on into the shoot. HAC1 therefore functions to reduce arsenate to arsenite in the outer cell layer of the root, facilitating efflux of arsenic as arsenite back into the soil to limit both its accumulation in the root and transport to the shoot. Arsenate reduction by HAC1 in the pericycle may play a role in limiting arsenic loading into the xylem. Loss of HAC1-encoded arsenic reduction leads to a significant increase in arsenic accumulation in shoots, causing an increased sensitivity to arsenate toxicity. We also confirmed the previous observation that the ACR2 arsenate reductase in A. thaliana plays no detectable role in arsenic metabolism. Furthermore, ACR2 does not interact epistatically with HAC1, since arsenic metabolism in the acr2 hac1 double mutant is disrupted in an identical manner to that described for the hac1 single mutant. Our identification of HAC1 and its associated natural variation provides an important new resource for the development of low arsenic-containing food such as rice.
Competing Interests: The authors have declared that no competing interests exist.

Comment in: PLoS Biol. 2014 Dec;12(12):e1002008. (PMID: 25464031)

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BB/H006303/1 United Kingdom Biotechnology and Biological Sciences Research Council; P42 ES007373 United States ES NIEHS NIH HHS; R01 GM078536 United States GM NIGMS NIH HHS; 2P4ES007373-19A1 United States ES NIEHS NIH HHS; BBS/E/C/00004960 United Kingdom BB_ Biotechnology and Biological Sciences Research Council; BB/L000113/1 United Kingdom Biotechnology and Biological Sciences Research Council; 2R01GM078536 United States GM NIGMS NIH HHS; BB/F004087/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council

0 (Arabidopsis Proteins)
EC 1.20.- (Arsenate Reductases)
EC 1.20.- (HAC1 protein, Arabidopsis)
N712M78A8G (Arsenic)

Date Created: 20141203 Date Completed: 20150730 Latest Revision: 20220129

20240829

PMC4251824

10.1371/journal.pbio.1002009

25464340