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

Titelangaben

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. Bd. 9 (2013) Heft 8 . - e1003707.
ISSN 1553-7404
DOI: https://doi.org/10.1371/journal.pgen.1003707

Abstract

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.

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Publikationsform: Artikel in einer Zeitschrift
Begutachteter Beitrag: Ja
Zusätzliche Informationen: 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
Institutionen der Universität: Fakultäten
Fakultäten > Fakultät für Biologie, Chemie und Geowissenschaften
Fakultäten > Fakultät für Biologie, Chemie und Geowissenschaften > Fachgruppe Biologie
Fakultäten > Fakultät für Biologie, Chemie und Geowissenschaften > Fachgruppe Biologie > Lehrstuhl Pflanzenphysiologie
Fakultäten > Fakultät für Biologie, Chemie und Geowissenschaften > Fachgruppe Biologie > Lehrstuhl Pflanzenphysiologie > Lehrstuhl Pflanzenphysiologie - Univ.-Prof. Dr. Stephan Clemens
Forschungseinrichtungen
Forschungseinrichtungen > Zentrale wissenschaftliche Einrichtungen
Forschungseinrichtungen > Zentrale wissenschaftliche Einrichtungen > Bayreuther Zentrum für Ökologie und Umweltforschung - BayCEER
Titel an der UBT entstanden: Nein
Themengebiete aus DDC: 500 Naturwissenschaften und Mathematik
500 Naturwissenschaften und Mathematik > 570 Biowissenschaften; Biologie
500 Naturwissenschaften und Mathematik > 580 Pflanzen (Botanik)
Eingestellt am: 29 Apr 2015 15:41
Letzte Änderung: 08 Aug 2023 11:24
URI: https://eref.uni-bayreuth.de/id/eprint/11599