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Human Molecular Genetics Advance Access published online on June 22, 2007
Human Molecular Genetics, doi:10.1093/hmg/ddm153
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© The Author 2007. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Rapid evolution of primate ESX1, an X-linked placenta- and testis-expressed homeobox gene

Xiaoxia Wang and Jianzhi Zhang*

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA

* Correspondence to: Jianzhi Zhang Department of Ecology and Evolutionary Biology, University of Michigan, 1075 Natural Science Building, 830 North University Avenue, Ann Arbor, MI 48109, Phone: 734-763-0527, Fax: 734-763-0544, Email: jianzhi{at}umich.edu

Received April 13, 2007; Revised June 1, 2007; Accepted June 14, 2007

Homeobox genes encode transcription factors that play important roles in various developmental processes and are usually evolutionarily conserved. Here we report a case of rapid evolution of a homeobox gene in humans and non-human primates. ESX1 is an X-linked homeobox gene primarily expressed in the placenta and testis, with physiological functions in placenta/fetus development and spermatogenesis. ESX1 is paternally imprinted in mice, but is not imprinted in humans. We provide evidence for a significantly higher nonsynonymous substitution rate than synonymous rate in ESX1 between humans and chimps as well as among a total of 15 primate species. Population genetic data also show signals of recent selective sweeps within humans. Positive selection appears to be concentrated in the C-terminal non-homeodomain region, which has been implicated in regulating human male germ cell division by prohibiting the degradation of cyclins. By contrast, mouse Esx1 has a substantively different C-terminal region subject to strong purifying selection. These and other results suggest that even the fundamental process of spermatogenesis has been targeted by positive selection in primate and human evolution and that mouse may not be a suitable model for studying human reproduction.


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