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

  • Among the rare colonizers of heavy-metal rich toxic soils, \(\textit {Arabidopsis halleri}\) is a compelling model extremophile, physiologically distinct from its sister species \(\textit {A. lyrata}\), and \(\textit {A. thaliana}\). Naturally selected metal hypertolerance and extraordinarily high leaf metal accumulation in \(\textit {A. halleri}\) both require \(\textit {Heavy Metal ATPase4 (HMA4)}\) encoding a \(P_{IB}\)-type ATPase that pumps \(Zn^{2+}\) and \(Cd^{2+}\) out of specific cell types. Strongly enhanced \(\it HMA4\) expression results from a combination of gene copy number expansion and \(\it cis\)-regulatory modifications, when compared to \(\textit {A. thaliana}\). These findings were based on a single accession of \(\textit {A. halleri}\). Few studies have addressed nucleotide sequence polymorphism at loci known to govern adaptations. We thus sequenced 13 DNA segments across the \(\it HMA4\) genomic region of multiple \(\textit {A. halleri}\) individuals from diverse habitats. Compared to control loci flanking the three tandem \(\it HMA4\) gene copies, a gradual depletion of nucleotide sequence diversity and an excess of low-frequency polymorphisms are hallmarks of positive selection in \(\it HMA4\) promoter regions, culminating at \(\it HMA4-3\). The accompanying hard selective sweep is segmentally eclipsed as a consequence of recurrent ectopic gene conversion among \(\it HMA4\) protein-coding sequences, resulting in their concerted evolution. Thus, \(\it HMA4\) 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 \(\textit {A. halleri}\), three genomic \(\it HMA4\) copies generate overall 20- to 130-fold higher transcript levels than in \(\textit {A. thaliana}\). Together, our observations constitute an unexpectedly complex profile of polymorphism resulting from natural selection for increased gene product dosage. We propose that these findings 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.

Download full text files

Export metadata

Additional Services

Share in Twitter Search Google Scholar
Metadaten
Author:Marc HanikenneGND, Jürgen KroymannGND, Aleksandra TrąmpczyńskaGND, María BernalORCiDGND, Patrick MotteGND, Stephan ClemensGND, Ute KrämerORCiDGND
URN:urn:nbn:de:hbz:294-73309
DOI:https://doi.org/10.1371/journal.pgen.1003707
Parent Title (English):PLoS genetics
Publisher:Public Library of Science
Place of publication:San Francisco
Document Type:Article
Language:English
Date of Publication (online):2020/07/14
Date of first Publication:2013/08/22
Publishing Institution:Ruhr-Universität Bochum, Universitätsbibliothek
Volume:9
Issue:8, Artikel e1003707
First Page:e1003707-1
Last Page:e1003707-13
Institutes/Facilities:Protein Research Department
Lehrstuhl für Molekulargenetik und Physiologie der Pflanzen
open_access (DINI-Set):open_access
Licence (English):License LogoCreative Commons - CC BY 4.0 - Attribution 4.0 International