Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4
Top Cited Papers
- 20 April 2008
- journal article
- letter
- Published by Springer Nature in Nature
- Vol. 453 (7193), 391-395
- https://doi.org/10.1038/nature06877
Abstract
Little is known about the types of mutations underlying the evolution of species-specific traits. The metal hyperaccumulator Arabidopsis halleri has the rare ability to colonize heavy-metal-polluted soils, and, as an extremophile sister species of Arabidopsis thaliana, it is a powerful model for research on adaptation1,2,3. A. halleri naturally accumulates and tolerates leaf concentrations as high as 2.2% zinc and 0.28% cadmium in dry biomass4. On the basis of transcriptomics studies, metal hyperaccumulation in A. halleri has been associated with more than 30 candidate genes that are expressed at higher levels in A. halleri than in A. thaliana4,5,6. Some of these genes have been genetically mapped to broad chromosomal segments of between 4 and 24 cM co-segregating with Zn and Cd hypertolerance7,8,9. However, the in planta loss-of-function approaches required to demonstrate the contribution of a given candidate gene to metal hyperaccumulation or hypertolerance have not been pursued to date. Using RNA interference to downregulate HMA4 (HEAVY METAL ATPASE 4) expression, we show here that Zn hyperaccumulation and full hypertolerance to Cd and Zn in A. halleri depend on the metal pump HMA4. Contrary to a postulated global trans regulatory factor governing high expression of numerous metal hyperaccumulation genes, we demonstrate that enhanced expression of HMA4 in A. halleri is attributable to a combination of modified cis-regulatory sequences and copy number expansion, in comparison to A. thaliana. Transfer of an A. halleri HMA4 gene to A. thaliana recapitulates Zn partitioning into xylem vessels and the constitutive transcriptional upregulation of Zn deficiency response genes characteristic of Zn hyperaccumulators. Our results demonstrate the importance of cis-regulatory mutations and gene copy number expansion in the evolution of a complex naturally selected extreme trait10. The elucidation of a natural strategy for metal hyperaccumulation enables the rational design of technologies for the clean-up of metal-contaminated soils and for bio-fortification.Keywords
This publication has 37 references indexed in Scilit:
- The Genetic Basis of Zinc Tolerance in the Metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): An Analysis of Quantitative Trait LociGenetics, 2007
- THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATIONEvolution, 2007
- A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPasePlant Physiology, 2007
- Zinc-Dependent Global Transcriptional Control, Transcriptional Deregulation, and Higher Gene Copy Number for Genes in Metal Homeostasis of the Hyperaccumulator Arabidopsis halleriPlant Physiology, 2006
- Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co‐segregate with zinc tolerance and account for high MTP1 transcript levelsThe Plant Journal, 2004
- NATURALLY OCCURRING GENETIC VARIATION IN ARABIDOPSIS THALIANAAnnual Review of Plant Biology, 2004
- Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factorsThe Plant Journal, 2003
- Cross‐species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleriThe Plant Journal, 2003
- Arabidopsis thaliana and its wild relatives: a model system for ecology and evolutionTrends in Ecology & Evolution, 2001
- Inventory of the Superfamily of P-Type Ion Pumps in ArabidopsisPlant Physiology, 2001