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

Chao, Dai-Yin; Chen, Yi; Chen, Jiugeng; Shi, Shulin; Chen, Ziru; Wang, Chengcheng; Danku, John; Zhao, Fang-Jie; Salt, David E.

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Authors

Dai-Yin Chao

Yi Chen

Jiugeng Chen

Shulin Shi

Ziru Chen

Chengcheng Wang

John Danku

Fang-Jie Zhao

David E. Salt



Abstract

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.

Citation

Chao, D.-Y., Chen, Y., Chen, J., Shi, S., Chen, Z., Wang, C., …Salt, D. E. (in press). Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biology, 12(12), Article e1002009. https://doi.org/10.1371/journal.pbio.1002009

Journal Article Type Article
Acceptance Date Oct 21, 2014
Online Publication Date Dec 2, 2014
Deposit Date Jan 26, 2017
Publicly Available Date Jan 26, 2017
Journal PLoS Biology
Print ISSN 1544-9173
Electronic ISSN 1545-7885
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 12
Issue 12
Article Number e1002009
DOI https://doi.org/10.1371/journal.pbio.1002009
Public URL https://nottingham-repository.worktribe.com/output/741708
Publisher URL http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1002009
Contract Date Jan 26, 2017

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