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

Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants.
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DOI:
10.1371/journal.pbio.1002009
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发表时间:
2014-12
期刊:
影响因子:
9.8
通讯作者:
Salt DE
Salt DE
中科院分区:
生物学1区
文献类型:
--
作者:
Chao DY;Chen Y;Chen J;Shi S;Chen Z;Wang C;Danku JM;Zhao FJ;Salt DE

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一项全基因组关联研究确定了植物中将砷酸盐转化为亚砷酸盐的酶,使其进入土壤,从而控制砷的积累。无机砷是一种致癌物质,通过食物(如大米)摄入无机砷对人体健康构成重大风险。植物通过化学反应将砷酸盐还原为亚砷酸盐。利用全基因组关联(GWA)定位控制拟南芥砷积累的自然变异的基因座,使我们能够确定这种减少所需的砷酸还原酶,我们将其命名为高砷含量1(HAC 1)。互补验证了身份的HAC 1,并在大肠杆菌中表达缺乏功能性的砷酸还原酶证实了砷酸还原酶活性的HAC 1。HAC 1蛋白在表皮、根的外细胞层以及围绕中央维管组织的周鞘细胞中积累。缺乏HAC 1的植物失去了从根部排出亚砷酸盐的能力,导致砷向中央维管组织和地上部的运输增加。因此,HAC 1的功能是在根的外细胞层中将砷酸盐还原为亚砷酸盐,促进砷以亚砷酸盐的形式回流到土壤中,以限制其在根中的积累和运输到地上部。砷酸盐减少由HAC 1在周皮层可能发挥作用,限制砷加载到木质部。失去的HAC 1编码的砷还原导致显着增加砷的积累在芽,造成增加的敏感性砷酸盐毒性。我们还证实了以前的观察,ACR 2砷酸还原酶在A。拟南芥在砷代谢中没有发挥可检测到的作用。此外,ACR 2不与HAC 1发生上位性相互作用,因为acr 2 hac 1双突变体中的砷代谢以与hac 1单突变体相同的方式被破坏。我们对HAC 1及其相关自然变异的鉴定为开发低砷食品(如大米)提供了重要的新资源。砷是一种人类致癌物质,从土壤中积累到许多不同的粮食作物中,当食用这些作物的食物时,它会显着增加癌症风险。植物自然地控制砷的积累量,首先通过化学方法将砷酸盐转化为亚砷酸盐,然后从根部排出回到土壤中。由于砷酸盐是磷酸盐的化学类似物,根中的砷酸盐转化为亚砷酸盐也可能阻止砷通过磷酸盐运输系统有效地运输到地上部。因此,砷酸盐的化学还原生成亚砷酸盐显然是植物解毒策略的关键组成部分。在这里,我们使用遗传方法来鉴定负责这一关键反应的酶--HAC 1。我们发现,HAC 1是负责砷酸还原酶活性在外层的根(表皮)和内层相邻的木质部(周壁)。在没有砷的情况下,根部向土壤中返回的砷较少,而芽中积累的砷高达300倍。这一知识为限制粮食作物中砷的积累创造了新的机会,从而有助于降低这种食物链污染物的癌症风险。
A genome-wide association study identifies the enzyme in plants that transforms arsenate into arsenite, allowing its extrusion into the soil and thereby controlling arsenic accumulation. 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. Arsenic is a human carcinogen that accumulates from soil into many different food crops, where it presents a significantly increased cancer risk when foods derived from these crops are consumed. Plants naturally control the amount of arsenic they accumulate by first chemically converting arsenate into arsenite, which is then extruded from the roots back into the soil. Because arsenate is a chemical analogue of phosphate, conversion of arsenate in the root to arsenite may also prevent arsenic being efficiently transported to the shoots via the phosphate transport system. The chemical reduction of arsenate to generate arsenite is therefore clearly a key component of a plant's detoxification strategy. Here, we use genetic methods to identify the enzyme responsible for this crucial reaction—HAC1. We show that HAC1 is responsible for arsenate reductase activity in both the outer layer of the root (epidermis) and the inner layer adjacent to the xylem (pericycle). In its absence, the roots return less arsenic to the soil and the shoots accumulate up to 300 times more arsenic. This knowledge creates new opportunities to limit arsenic accumulation in food crops, thereby helping to reduce the cancer risk from this food-chain contaminant.
DOI: 10.1371/journal.pgen.1001193
发表时间: 2010-11-11
期刊: PLoS genetics
影响因子: 4.5
作者:
Baxter I;Brazelton JN;Yu D;Huang YS;Lahner B;Yakubova E;Li Y;Bergelson J;Borevitz JO;Nordborg M;Vitek O;Salt DE
通讯作者: Salt DE
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发表时间: 2009-08-01
影响因子: 3.8
作者:
Gregus, Zoltan;Roos, Goedele;Nemeti, Balazs
通讯作者: Nemeti, Balazs
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发表时间: 2011-10
期刊: The New phytologist
影响因子: --
作者:
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通讯作者: Meharg AA
DOI: 10.1371/journal.pgen.1002923
发表时间: 2012-09
期刊: PLoS genetics
影响因子: 4.5
作者:
Chao DY;Silva A;Baxter I;Huang YS;Nordborg M;Danku J;Lahner B;Yakubova E;Salt DE
通讯作者: Salt DE
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发表时间: 2012
期刊: PLoS genetics
影响因子: 4.5
作者:
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通讯作者: Maloof JN