MBE Advance Access published online on July 23, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm153
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Research Article |
Origins of New Male Germline Functions from X-derived Autosomal Retrogenes in the Mouse
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* Department of Ecology and Evolution, University of Chicago, Illinois 60637, USA
Institute of Zoology, National Taiwan University, Taipei 106, Taiwan
Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, Maryland 20892, USA
¶ National Institute of Genetics, Yata-1111, Mishima, Shizuoka-ken 411-8540, Japan
RIKEN BioResources Center, 3-1-1 Koyadai,Tsukuba-shi, Ibaraki 305-0074, Japan
|| Department of Life Science, National Taiwan University, Taipei 106, Taiwan
1 To whom correspondence should be addressed. Manyuan Long, mlong{at}uchicago.edu; Hon-Tsen Yu, ayu{at}ntu.edu.tw
Received for publication May 2, 2007. Revision received July 12, 2007. Accepted for publication July 16, 2007.
Recent literature demonstrates that retrogenes tend to leave the X chromosome and integrate onto the autosomes and evolve male-biased expression patterns. Several selection-based evolutionary mechanisms have been proposed to explain this observation. Testing these selection-based models requires examining the evolutionary history and functional properties of new retrogenes, particularly those that show evidence of directional movement between the X and the autosomes (X-related retrogenes). This includes autosomal retrogenes with parental paralogs on the X chromosome (X-derived autosomal retrogenes) and those retrogenes integrated onto the X chromosomes (X-linked retrogenes). In order to understand why retrogenes tend to move non-randomly in genomes, we examined the expression patterns and evolutionary mechanisms concerning gene pairs having young retrogenes —originating less than 20 million years ago (after mouse-rat split). We demonstrate that these X-derived autosomal retrogenes evolved a more restricted male-biased expression pattern: they are expressed exclusively or predominantly in the testis, in particular, during the late stages of spermatogenesis. In contrast, the parental counterparts have relatively broad expression patterns in various tissues and spermatogenetic stages. We further observed that positive selection was targeting these X-derived autosomal retrogenes with novel male-biased expression patterns. This suggests that such retrogenes evolved new male germline functions that may be complementary to the functions of the parental paralogs, which themselves contribute little during spermatogenesis. Such evolutionary changes may be beneficial to the populations. Furthermore, most identified X-related retrogenes have recruited novel adjacent sequences as their untranslated regions (UTRs), suggesting that these UTRs, acquired de novo, may play an important role in establishing new regulatory mechanisms to carry out the new male germline functions.
Key Words: Mouse • Retroposition • Spermatogenesis • Male functions
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