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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPase^1,[OA]

Laboratoire de Physiologie et de Génétique moléculaire des Plantes, Université Libre de Bruxelles, B–1050 Brussels, Belgium (M.C., G.W., S.A., N.V.); Laboratoire de Génétique et Evolution des Populations Végétales, Unité Mixte de Recherche Centre National de la Recherche Scientifique 8016, FR Centre National de la Recherche Scientifique 1818, Université de Lille 1, F–59655 Villeneuve d'Ascq cedex, France (G.W., N.R., P.S.-L.); and Laboratory of Plant Cell and Molecular Biology and Center for Assistance in Technology of Microscopy, University of Liège, B–4000 Liege, Belgium (P.M.)

Cadmium (Cd) tolerance seems to be a constitutive species-level trait in Arabidopsis halleri sp. halleri. Therefore, an interspecific cross was made between A. halleri and its closest nontolerant interfertile relative, Arabidopsis lyrata sp. petraea, and a first-generation backcross population (BC1) was used to map quantitative trait loci (QTL) for Cd tolerance. Three QTL were identified, which explained 43%, 24%, and 16% of the phenotypic variation in the mapping population. Heavy metal transporting ATPases4 (HMA4), encoding a predicted heavy metal ATPase, colocalized with the peak of the major QTL Cdtol-1 and was consequently further studied. HMA4 transcripts levels were higher in the roots and the shoots of A. halleri than in A. lyrata sp. petraea. Furthermore, HMA4 was also more highly expressed in all BC1 genotypes harboring the HMA4 A. halleri allele at the QTL Cdtol-1, independently of the presence of an A. halleri allele at the two other QTL. Overexpression of AhHMA4 in yeast (Saccharomyces cerevisiae) supported a role of HMA4 in zinc (Zn) and Cd transport by reducing the Cd and Zn contents of the yeast cells. In epidermal tobacco (Nicotiana tabacum) cells, AhHMA4:green fluorescent protein was clearly localized in the plasma membrane. Taken together, all available data point to the elevated expression of HMA4 P_1B-type ATPase as an efficient mechanism for improving Cd/Zn tolerance in plants under conditions of Cd/Zn excess by maintaining low cellular Cd²⁺ and Zn²⁺ concentrations in the cytoplasm.

² These authors contributed equally to the article.

³ Present address: Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Nathalie Verbruggen (nverbru{at}ulb.ac.be).

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www.plantphysiol.org/cgi/doi/10.1104/pp.106.095133

^* Corresponding author; e-mail nverbru{at}ulb.ac.be; fax 32–2–650–54–21.

Received December 20, 2006; accepted April 5, 2007; published April 13, 2007.

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