Plant Cell Advance Online Publication
Published on July 7, 2006; 10.1105/tpc.106.041905
Received February 13, 2006
Returned for revision April 15, 2006
Accepted June 8, 2006
High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes
Wen Wang 1, Hongkun Zheng 2, Chuanzhu Fan 3, Jun Li 4, Junjie Shi 5, Zhengqiu Cai 4, Guojie Zhang 6, Dongyuan Liu 4, Jianguo Zhang 4, Søren Vang 7, Zhike Lu 4, Gane Ka-Shu Wong 4, Manyuan Long 3*, and Jun Wang 8
1 CAS-Max-Plank Junior Research Group, Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China
2 Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China; Department of Biochemistry and Molecular Biology, University of Southern Denmark, DK-5230, Odense M, Denmark
3 Department of Ecology and Evolution, University of Chicago, Chicago 60637, Illinois
4 Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China
5 Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China; Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan 250014, China
6 CAS-Max-Plank Junior Research Group, Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China; Graduate School of Chinese Academy Sciences, Beijing 100039, China
7 Institute of Human Genetics, University of Aarhus, DK-8000, Aarhus C, Denmark
8 Beijing Genomics Institute, Chinese Academy of Sciences, Beijing 101300, China; Department of Biochemistry and Molecular Biology, University of Southern Denmark, DK-5230, Odense M, Denmark; Institute of Human Genetics, University of Aarhus, DK-8000, Aarhus C, Denmark
* To whom correspondence should be addressed. E-mail: mlong{at}uchicago.edu.
Retroposition is widely found to play essential roles in origination of new mammalian and other animal genes. However, the scarcity of retrogenes in plants has led to the assumption that plant genomes rarely evolve new gene duplicates by retroposition, despite abundant retrotransposons in plants and a reported long terminal repeat (LTR) retrotransposon-mediated mechanism of retroposing cellular genes in maize (Zea mays). We show extensive retropositions in the rice (Oryza sativa) genome, with 1235 identified primary retrogenes. We identified 27 of these primary retrogenes within LTR retrotransposons, confirming a previously observed role of retroelements in generating plant retrogenes. Substitution analyses revealed that the vast majority are subject to negative selection, suggesting, along with expression data and evidence of age, that they are likely functional retrogenes. In addition, 42% of these retrosequences have recruited new exons from flanking regions, generating a large number of chimerical genes. We also identified young chimerical genes, suggesting that gene origination through retroposition is ongoing, with a rate an order of magnitude higher than the rate in primates. Finally, we observed that retropositions have followed an unexpected spatial pattern in which functional retrogenes avoid centromeric regions, while retropseudogenes are randomly distributed. These observations suggest that retroposition is an important mechanism that governs gene evolution in rice and other grass species.
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