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First published online July 14, 2006; 10.1104/pp.105.076232

Plant Physiology 142:148-167 (2006)
© 2006 American Society of Plant Biologists

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GENETICS, GENOMICS, AND MOLECULAR EVOLUTION

Zinc-Dependent Global Transcriptional Control, Transcriptional Deregulation, and Higher Gene Copy Number for Genes in Metal Homeostasis of the Hyperaccumulator Arabidopsis halleri1,[W]

Ina N. Talke2, Marc Hanikenne2 and Ute Krämer*

Max Planck Institute of Molecular Plant Physiology, D–14476 Potsdam-Golm, Germany

The metal hyperaccumulator Arabidopsis halleri exhibits naturally selected zinc (Zn) and cadmium (Cd) hypertolerance and accumulates extraordinarily high Zn concentrations in its leaves. With these extreme physiological traits, A. halleri phylogenetically belongs to the sister clade of Arabidopsis thaliana. Using a combination of genome-wide cross species microarray analysis and real-time reverse transcription-PCR, a set of candidate genes is identified for Zn hyperaccumulation, Zn and Cd hypertolerance, and the adjustment of micronutrient homeostasis in A. halleri. Eighteen putative metal homeostasis genes are newly identified to be more highly expressed in A. halleri than in A. thaliana, and 11 previously identified candidate genes are confirmed. The encoded proteins include HMA4, known to contribute to root-shoot transport of Zn in A. thaliana. Expression of either AtHMA4 or AhHMA4 confers cellular Zn and Cd tolerance to yeast (Saccharomyces cerevisiae). Among further newly implicated proteins are IRT3 and ZIP10, which have been proposed to contribute to cytoplasmic Zn influx, and FRD3 required for iron partitioning in A. thaliana. In A. halleri, the presence of more than a single genomic copy is a hallmark of several highly expressed candidate genes with possible roles in metal hyperaccumulation and metal hypertolerance. Both A. halleri and A. thaliana exert tight regulatory control over Zn homeostasis at the transcript level. Zn hyperaccumulation in A. halleri involves enhanced partitioning of Zn from roots into shoots. The transcriptional regulation of marker genes suggests that in the steady state, A. halleri roots, but not the shoots, act as physiologically Zn deficient under conditions of moderate Zn supply.


1 This work was supported by the Deutsche Forschungsgemeinschaft (Kr 1967/3), the European Union (Research Training Network METALHOME, HPRN–CT–2002–00243), the German Federal Ministry of Education and Research (Biofuture 0311877), and the Max Planck Institute of Molecular Plant Physiology.

2 These authors contributed equally to the paper.

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: Ute Krämer (kraemer{at}mpimp-golm.mpg.de).

[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.105.076232

* Corresponding author; e-mail kraemer{at}mpimp-golm.mpg.de; fax 49–331–5678–408.

Received December 23, 2005; accepted July 4, 2006.




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