High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes
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...
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Veröffentlicht in: | The Plant cell 2006-08, Vol.18 (8), p.1791-1802 |
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creator | Wang, Wen Zheng, Hongkun Fan, Chuanzhu Li, Jun Shi, Junjie Cai, Zhengqiu Zhang, Guojie Liu, Dongyuan Zhang, Jianguo Vang, Søren Lu, Zhike Wong, Gane Ka-Shu Long, Manyuan Wang, Jun |
description | 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. |
doi_str_mv | 10.1105/tpc.106.041905 |
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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.</description><identifier>ISSN: 1040-4651</identifier><identifier>ISSN: 1532-298X</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.106.041905</identifier><identifier>PMID: 16829590</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Complementary DNA ; Corn ; Drosophila ; duplicate genes ; Evolution ; Evolution, Molecular ; exons ; Gene Order ; Genes ; Genes, Plant ; Genome, Plant ; Genomes ; Genomics ; grasses ; Molecular Sequence Data ; Mutant Chimeric Proteins - genetics ; Oryza - genetics ; Oryza sativa ; Primates ; Pseudogenes ; recombinant fusion proteins ; Retroelements - physiology ; Retrotransposons ; Rice ; terminal repeat sequences ; Zea mays</subject><ispartof>The Plant cell, 2006-08, Vol.18 (8), p.1791-1802</ispartof><rights>Copyright 2006 American Society of Plant Biologists</rights><rights>Copyright American Society of Plant Physiologists Aug 2006</rights><rights>Copyright © 2006, American Society of Plant Biologists</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c591t-a157f7120edeaa0d2e0e3aa1d09f7b95b0b048d1c3244af251550558d5b2c1863</citedby><cites>FETCH-LOGICAL-c591t-a157f7120edeaa0d2e0e3aa1d09f7b95b0b048d1c3244af251550558d5b2c1863</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/20076738$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/20076738$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16829590$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Wen</creatorcontrib><creatorcontrib>Zheng, Hongkun</creatorcontrib><creatorcontrib>Fan, Chuanzhu</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Shi, Junjie</creatorcontrib><creatorcontrib>Cai, Zhengqiu</creatorcontrib><creatorcontrib>Zhang, Guojie</creatorcontrib><creatorcontrib>Liu, Dongyuan</creatorcontrib><creatorcontrib>Zhang, Jianguo</creatorcontrib><creatorcontrib>Vang, Søren</creatorcontrib><creatorcontrib>Lu, Zhike</creatorcontrib><creatorcontrib>Wong, Gane Ka-Shu</creatorcontrib><creatorcontrib>Long, Manyuan</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><title>High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>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.</description><subject>Complementary DNA</subject><subject>Corn</subject><subject>Drosophila</subject><subject>duplicate genes</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>exons</subject><subject>Gene Order</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomics</subject><subject>grasses</subject><subject>Molecular Sequence Data</subject><subject>Mutant Chimeric Proteins - genetics</subject><subject>Oryza - genetics</subject><subject>Oryza sativa</subject><subject>Primates</subject><subject>Pseudogenes</subject><subject>recombinant fusion proteins</subject><subject>Retroelements - physiology</subject><subject>Retrotransposons</subject><subject>Rice</subject><subject>terminal repeat sequences</subject><subject>Zea mays</subject><issn>1040-4651</issn><issn>1532-298X</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkUtvEzEUhS0EoqWwZQeMWLCbcK-f4w0SiqBBqlRUqMTO8sx4EkeZcbAdpP57HCYqjw0rX_l893kIeY6wQATxNu-7BYJcAEcN4gE5R8FoTXXz7WGJgUPNpcAz8iSlLQCgQv2YnKFsqBYazslq5deb6sZmV4WhWm786KLvqks3ueo6-rWfbPZhqtq76sblGPYh-V8ffqo-7-yUj2gYXXpKHg12l9yz03tBbj9--Lpc1VfXl5-W76_qTmjMtUWhBoUUXO-shZ46cMxa7EEPqtWihRZ402PHKOd2oAKFACGaXrS0w0ayC_Jurrs_tKPrOzflaHdmH_1o450J1pu_lclvzDr8MOUwTCtdCrw5FYjh-8GlbEafOrcry7hwSEY2itPS9L8galbOKXkBX_8DbsMhTuUKhmKjVOl6nHsxQ10MKUU33I-MYI5WmmJliaWZrSwJL_9c9Dd-8q4AL2Zgm3KI9zoFUFKxpuivZn2wwdh19MncfqGADBA0p5Kyn04urEM</recordid><startdate>20060801</startdate><enddate>20060801</enddate><creator>Wang, Wen</creator><creator>Zheng, Hongkun</creator><creator>Fan, Chuanzhu</creator><creator>Li, Jun</creator><creator>Shi, Junjie</creator><creator>Cai, Zhengqiu</creator><creator>Zhang, Guojie</creator><creator>Liu, Dongyuan</creator><creator>Zhang, Jianguo</creator><creator>Vang, Søren</creator><creator>Lu, Zhike</creator><creator>Wong, Gane Ka-Shu</creator><creator>Long, Manyuan</creator><creator>Wang, Jun</creator><general>American Society of Plant Biologists</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>S0X</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060801</creationdate><title>High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes</title><author>Wang, Wen ; Zheng, Hongkun ; Fan, Chuanzhu ; Li, Jun ; Shi, Junjie ; Cai, Zhengqiu ; Zhang, Guojie ; Liu, Dongyuan ; Zhang, Jianguo ; Vang, Søren ; Lu, Zhike ; Wong, Gane Ka-Shu ; Long, Manyuan ; Wang, Jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c591t-a157f7120edeaa0d2e0e3aa1d09f7b95b0b048d1c3244af251550558d5b2c1863</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Complementary DNA</topic><topic>Corn</topic><topic>Drosophila</topic><topic>duplicate genes</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>exons</topic><topic>Gene Order</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Genome, Plant</topic><topic>Genomes</topic><topic>Genomics</topic><topic>grasses</topic><topic>Molecular Sequence Data</topic><topic>Mutant Chimeric Proteins - genetics</topic><topic>Oryza - genetics</topic><topic>Oryza sativa</topic><topic>Primates</topic><topic>Pseudogenes</topic><topic>recombinant fusion proteins</topic><topic>Retroelements - physiology</topic><topic>Retrotransposons</topic><topic>Rice</topic><topic>terminal repeat sequences</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Wen</creatorcontrib><creatorcontrib>Zheng, Hongkun</creatorcontrib><creatorcontrib>Fan, Chuanzhu</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Shi, Junjie</creatorcontrib><creatorcontrib>Cai, Zhengqiu</creatorcontrib><creatorcontrib>Zhang, Guojie</creatorcontrib><creatorcontrib>Liu, Dongyuan</creatorcontrib><creatorcontrib>Zhang, Jianguo</creatorcontrib><creatorcontrib>Vang, Søren</creatorcontrib><creatorcontrib>Lu, Zhike</creatorcontrib><creatorcontrib>Wong, Gane Ka-Shu</creatorcontrib><creatorcontrib>Long, Manyuan</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Wen</au><au>Zheng, Hongkun</au><au>Fan, Chuanzhu</au><au>Li, Jun</au><au>Shi, Junjie</au><au>Cai, Zhengqiu</au><au>Zhang, Guojie</au><au>Liu, Dongyuan</au><au>Zhang, Jianguo</au><au>Vang, Søren</au><au>Lu, Zhike</au><au>Wong, Gane Ka-Shu</au><au>Long, Manyuan</au><au>Wang, Jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2006-08-01</date><risdate>2006</risdate><volume>18</volume><issue>8</issue><spage>1791</spage><epage>1802</epage><pages>1791-1802</pages><issn>1040-4651</issn><issn>1532-298X</issn><eissn>1532-298X</eissn><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><cop>England</cop><pub>American Society of Plant Biologists</pub><pmid>16829590</pmid><doi>10.1105/tpc.106.041905</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Complementary DNA Corn Drosophila duplicate genes Evolution Evolution, Molecular exons Gene Order Genes Genes, Plant Genome, Plant Genomes Genomics grasses Molecular Sequence Data Mutant Chimeric Proteins - genetics Oryza - genetics Oryza sativa Primates Pseudogenes recombinant fusion proteins Retroelements - physiology Retrotransposons Rice terminal repeat sequences Zea mays |
title | High Rate of Chimeric Gene Origination by Retroposition in Plant Genomes |
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