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PMID: 19997497 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa.

PLoS genetics ·Vol. 5 ·No. 12 ·2009-12-00 ·Pages e1000753

Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, Phadnis N, Beatson SA, Lunter G, Malik HS, Ponting CP

Abstract

The onset of prezygotic and postzygotic barriers to gene flow between populations is a hallmark of speciation. One of the earliest postzygotic isolating barriers to arise between incipient species is the sterility of the heterogametic sex in interspecies' hybrids. Four genes that underlie hybrid sterility have been identified in animals: Odysseus, JYalpha, and Overdrive in Drosophila and Prdm9 (Meisetz) in mice. Mouse Prdm9 encodes a protein with a KRAB motif, a histone methyltransferase domain and several zinc fingers. The difference of a single zinc finger distinguishes Prdm9 alleles that cause hybrid sterility from those that do not. We find that concerted evolution and positive selection have rapidly altered the number and sequence of Prdm9 zinc fingers across 13 rodent genomes. The patterns of positive selection in Prdm9 zinc fingers imply that rapid evolution has acted on the interface between the Prdm9 protein and the DNA sequences to which it binds. Similar patterns are apparent for Prdm9 zinc fingers for diverse metazoans, including primates. Indeed, allelic variation at the DNA-binding positions of human PRDM9 zinc fingers show significant association with decreased risk of infertility. Prdm9 thus plays a role in determining male sterility both between species (mouse) and within species (human). The recurrent episodes of positive selection acting on Prdm9 suggest that the DNA sequences to which it binds must also be evolving rapidly. Our findings do not identify the nature of the underlying DNA sequences, but argue against the proposed role of Prdm9 as an essential transcription factor in mouse meiosis. We propose a hypothetical model in which incompatibilities between Prdm9-binding specificity and satellite DNAs provide the molecular basis for Prdm9-mediated hybrid sterility. We suggest that Prdm9 should be investigated as a candidate gene in other instances of hybrid sterility in metazoans.

MeSH Terms
Amino Acid Sequence Animals Base Sequence DNA, Satellite/genetics Evolution, Molecular Genetic Speciation Histone-Lysine N-Methyltransferase/chemistry,genetics Humans Models, Biological Molecular Sequence Data Phylogeny Primates/genetics Rodentia/genetics Selection, Genetic Zinc Fingers/genetics
Chemicals
DNA, Satellite Histone-Lysine N-Methyltransferase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Oliver Peter L
Medical Research Council Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom.
Goodstadt Leo
Bayes Joshua J
Birtle Zoë
Roach Kevin C
Phadnis Nitin
Beatson Scott A
Lunter Gerton
Malik Harmit S
Ponting Chris P
Conflict of Interest

The authors have declared that no competing interests exist.

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Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
DOI
10.1371/journal.pgen.1000753
Published
2009-12-00
Epub
2009-00-04
Pages
e1000753
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC2779102
Subset
IM
Grants
Medical Research Council · G0501331 · United Kingdom
Medical Research Council · MC_U137761446 · United Kingdom
NIGMS NIH HHS · T32 GM07270 · United States
NIGMS NIH HHS · T32 GM007270 · United States
NIGMS NIH HHS · R01 GM074108-05 · United States
NIGMS NIH HHS · R01 GM074108 · United States
NIGMS NIH HHS · R01-GM74108 · United States
External Links
PubMed source DOI: 10.1371/journal.pgen.1000753 PMC Full Text View journal details
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