High rate of chimeric gene origination by retroposition in plant genomes.
Journal: 2006/November - Plant Cell
ISSN: 1040-4651
Abstract:
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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Plant Cell 18(8): 1791-1802

High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes<sup><a href="#fn2" rid="fn2" class=" fn">[W]</a></sup>

+5 authors
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
Department of Biochemistry and Molecular Biology, University of Southern Denmark, DK-5230, Odense M, Denmark
Department of Ecology and Evolution, University of Chicago, Chicago 60637, Illinois
Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan 250014, China
Graduate School of Chinese Academy Sciences, Beijing 100039, China
Institute of Human Genetics, University of Aarhus, DK-8000, Aarhus C, Denmark
These authors contributed equally to this work.
To whom correspondence should be addressed. E-mail ude.ogacihcu@gnolm or nc.gro.scimoneg@jgnaw; fax 773-702-9740.
Received 2006 Feb 13; Revised 2006 Apr 15; Accepted 2006 Jun 8.

Abstract

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.

Abstract

RG-Ψ refers to retroseudogenes, and RG-f refers to intact retrogenes. RG, retrogene.

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Acknowledgments

This work was sponsored by the CAS-Max-Planck Society Fellowship, a Chinese Academy of Sciences key project grant (KSCX2-SW-121), a National Science Foundation of China (NSFC) award (30325016) to distinguished young scientists, and a NSFC key grant (30430400) to W.W. Funding was from the Chinese Academy of Sciences (GJHZ0518), the Ministry of Science and Technology of China (CNG1-04-15-7A), the National Natural Science Foundation of China (90208019, 90403130, and 30221004), the China National Grid, the Danish Platform for Integrative Biology, Ole Rømer grants from the Danish Natural Science Research Council to J.W., a National Science Foundation CAREER award (MCB0238168), a National Institutes of Health R01 grant (R01GM065429-01A1), and from the Packard Fellowship for Science and Engineering from the David and Lucile Packard Foundation to M.L. We thank two anonymous reviewers for their generous and insightful suggestions. We also appreciate the valuable discussions with Elizabeth Kellogg (University of Missouri, St. Louis, MO) and Ming-Che Shih (University of Iowa, Iowa City, IA).

Acknowledgments

Notes

The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Wen Wang (nc.ca.zik.liam@gnaww), Manyuan Long (ude.ogacihcu@gnolm), and Jun Wang (nc.gro.scimoneg@jgnaw).

Online version contains Web-only data.

Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.106.041905.

Notes
The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Wen Wang (nc.ca.zik.liam@gnaww), Manyuan Long (ude.ogacihcu@gnolm), and Jun Wang (nc.gro.scimoneg@jgnaw).Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.106.041905.
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