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Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation

Title data

Hanikenne, Marc ; Kroymann, Jürgen ; Trampczynska, Aleksandra ; Bernal, María ; Motte, Patrick ; Clemens, Stephan ; Krämer, Ute:
Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation.
In: PLoS Genetics. Vol. 9 (August 2013) Issue 8 . - Eintrag 1003707 (13 Seiten).
ISSN 1553-7404
DOI: https://doi.org/10.1371/journal.pgen.1003707

Abstract in another language

Among the rare colonizers of heavy-metal rich toxic soils, Arabidopsis halleri is a compelling model extremophile, physiologically distinct from its sister species A. lyrata, and A. thaliana. Both naturally selected metal hypertolerance and extraordinarily high leaf metal accumulation in A. halleri require Heavy Metal ATPase4 (HMA4) encoding a PIB-type ATPase that pumps Zn2+ and Cd2+ out of specific cell types. Strongly enhanced HMA4 expression results from a combination of gene copy number expansion and cis-regulatory modifications, when compared to A. thaliana. These findings were based on a single accession of A. halleri. Few studies have addressed nucleotide sequence polymorphism at loci known to govern adaptations. We thus sequenced 13 DNA segments across the HMA4 genomic region of multiple A. halleri individuals from diverse habitats. Compared to control loci flanking the three tandem HMA4 gene copies, a gradual depletion of nucleotide sequence diversity and an excess of low-frequency polymorphisms are hallmarks of positive selection in HMA4 promoter regions, culminating at HMA4-3. The accompanying hard selective sweep is segmentally eclipsed as a consequence of recurrent ectopic gene conversion among HMA4 protein-coding sequences, resulting in their concerted evolution. Thus, HMA4 coding sequences exhibit a network-like genealogy and locally enhanced nucleotide sequence diversity within each copy, accompanied by lowered sequence divergence between paralogs in any given individual. Quantitative PCR corroborated that, across A. halleri, three genomic HMA4 copies generate overall 20- to 130-fold higher transcript levels than in A. thaliana. Together, our observations constitute an unexpectedly complex profile of polymorphism resulting from natural selection for increased gene product dosage. We propose that these finding are paradigmatic of a category of multi-copy genes from a broad range of organisms. Our results emphasize that enhanced gene product dosage, in addition to neo- and sub-functionalization, can account for the genomic maintenance of gene duplicates underlying environmental adaptation.

Further data

Item Type: Article in a journal
Refereed: Yes
Additional notes: BAYCEER116864
Keywords: Arabidopsis; Arabidopsis Proteins; Gene Expression Regulation; Plant; Cadmium; Plant Leaves; Promoter Regions; Genetic; Multigene Family; Adaptation; Physiological; Gene Dosage; Adenosine Triphosphatases; Zinc; Gene Conversion
Institutions of the University: Faculties
Faculties > Faculty of Biology, Chemistry and Earth Sciences
Faculties > Faculty of Biology, Chemistry and Earth Sciences > Department of Biology
Faculties > Faculty of Biology, Chemistry and Earth Sciences > Department of Biology > Chair Plant Physiology
Faculties > Faculty of Biology, Chemistry and Earth Sciences > Department of Biology > Chair Plant Physiology > Chair Plant Physiology - Univ.-Prof. Dr. Stephan Clemens
Research Institutions
Research Institutions > Research Centres
Research Institutions > Research Centres > Bayreuth Center of Ecology and Environmental Research- BayCEER
Result of work at the UBT: No
DDC Subjects: 500 Science
500 Science > 570 Life sciences, biology
500 Science > 580 Plants (Botany)
Date Deposited: 29 Apr 2015 15:41
Last Modified: 10 Jan 2018 10:15
URI: https://eref.uni-bayreuth.de/id/eprint/11599