Intracellular Gene Transfer in Action: Dual Transcription and Multiple Silencings of Nuclear and Mitochondrial cox2 Genes in Legumes
The respiratory gene cox2, normally present in the mitochondrion, was previously shown to have been functionally transferred to the nucleus during flowering plant evolution, possibly during the diversification of legumes. To search for novel intermediate stages in the process of intracellular gene t...
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creator | Adams, Keith L. Song, Keming Roessler, Philip G. Nugent, Jacqueline M. Doyle, Jane L. Doyle, Jeff J. Palmer, Jeffrey D. |
description | The respiratory gene cox2, normally present in the mitochondrion, was previously shown to have been functionally transferred to the nucleus during flowering plant evolution, possibly during the diversification of legumes. To search for novel intermediate stages in the process of intracellular gene transfer and to assess the evolutionary timing and frequency of cox2 transfer, activation, and inactivation, we examined nuclear and mitochondrial (mt) cox2 presence and expression in over 25 legume genera and mt cox2 presence in 392 genera. Transfer and activation of cox2 appear to have occurred during recent legume evolution, more recently than previously inferred. Many intermediate stages of the gene transfer process are represented by cox2 genes in the studied legumes. Nine legumes contain intact copies of both nuclear and mt cox2, although transcripts could not be detected for some of these genes. Both cox2 genes are transcribed in seven legumes that are phylogenetically interspersed with species displaying only nuclear or mt cox2 expression. Inactivation of cox2 in each genome has taken place multiple times and in a variety of ways, including loss of detectable transcripts or transcript editing and partial to complete gene loss. Phylogenetic evidence shows about the same number (3-5) of separate inactivations of nuclear and mt cox2, suggesting that there is no selective advantage for a mt vs. nuclear location of cox2 in plants. The current distribution of cox2 presence and expression between the nucleus and mitochondrion in the studied legumes is probably the result of chance mutations silencing either cox2 gene. |
doi_str_mv | 10.1073/pnas.96.24.13863 |
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To search for novel intermediate stages in the process of intracellular gene transfer and to assess the evolutionary timing and frequency of cox2 transfer, activation, and inactivation, we examined nuclear and mitochondrial (mt) cox2 presence and expression in over 25 legume genera and mt cox2 presence in 392 genera. Transfer and activation of cox2 appear to have occurred during recent legume evolution, more recently than previously inferred. Many intermediate stages of the gene transfer process are represented by cox2 genes in the studied legumes. Nine legumes contain intact copies of both nuclear and mt cox2, although transcripts could not be detected for some of these genes. Both cox2 genes are transcribed in seven legumes that are phylogenetically interspersed with species displaying only nuclear or mt cox2 expression. Inactivation of cox2 in each genome has taken place multiple times and in a variety of ways, including loss of detectable transcripts or transcript editing and partial to complete gene loss. Phylogenetic evidence shows about the same number (3-5) of separate inactivations of nuclear and mt cox2, suggesting that there is no selective advantage for a mt vs. nuclear location of cox2 in plants. The current distribution of cox2 presence and expression between the nucleus and mitochondrion in the studied legumes is probably the result of chance mutations silencing either cox2 gene.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.96.24.13863</identifier><identifier>PMID: 10570164</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Biological Sciences ; Botany ; Cell Nucleus ; Complementary DNA ; cox2 gene ; DNA ; Electron Transport Complex IV - genetics ; Evolution ; Fabaceae - enzymology ; Fabaceae - genetics ; Genes ; Genes, Plant ; Genetic hybridization ; Genomes ; Legumes ; Leguminosae ; Mitochondria - genetics ; Molecular Sequence Data ; Plant Proteins - genetics ; Plants, Medicinal ; Recombination, Genetic ; Reverse transcriptase polymerase chain reaction ; RNA ; Soybeans ; Transcription, Genetic</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1999-11, Vol.96 (24), p.13863-13868</ispartof><rights>Copyright 1993-1999 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Nov 23, 1999</rights><rights>Copyright © 1999, The National Academy of Sciences 1999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-91d9e7fa931e7f398bab728e4f4b7756ca5f39a51299f3161024a31d8684df813</citedby><cites>FETCH-LOGICAL-c525t-91d9e7fa931e7f398bab728e4f4b7756ca5f39a51299f3161024a31d8684df813</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/96/24.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/121313$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/121313$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10570164$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Adams, Keith L.</creatorcontrib><creatorcontrib>Song, Keming</creatorcontrib><creatorcontrib>Roessler, Philip G.</creatorcontrib><creatorcontrib>Nugent, Jacqueline M.</creatorcontrib><creatorcontrib>Doyle, Jane L.</creatorcontrib><creatorcontrib>Doyle, Jeff J.</creatorcontrib><creatorcontrib>Palmer, Jeffrey D.</creatorcontrib><title>Intracellular Gene Transfer in Action: Dual Transcription and Multiple Silencings of Nuclear and Mitochondrial cox2 Genes in Legumes</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The respiratory gene cox2, normally present in the mitochondrion, was previously shown to have been functionally transferred to the nucleus during flowering plant evolution, possibly during the diversification of legumes. 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Inactivation of cox2 in each genome has taken place multiple times and in a variety of ways, including loss of detectable transcripts or transcript editing and partial to complete gene loss. Phylogenetic evidence shows about the same number (3-5) of separate inactivations of nuclear and mt cox2, suggesting that there is no selective advantage for a mt vs. nuclear location of cox2 in plants. The current distribution of cox2 presence and expression between the nucleus and mitochondrion in the studied legumes is probably the result of chance mutations silencing either cox2 gene.</description><subject>Biological Sciences</subject><subject>Botany</subject><subject>Cell Nucleus</subject><subject>Complementary DNA</subject><subject>cox2 gene</subject><subject>DNA</subject><subject>Electron Transport Complex IV - genetics</subject><subject>Evolution</subject><subject>Fabaceae - enzymology</subject><subject>Fabaceae - genetics</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genetic hybridization</subject><subject>Genomes</subject><subject>Legumes</subject><subject>Leguminosae</subject><subject>Mitochondria - genetics</subject><subject>Molecular Sequence Data</subject><subject>Plant Proteins - genetics</subject><subject>Plants, Medicinal</subject><subject>Recombination, Genetic</subject><subject>Reverse transcriptase polymerase chain reaction</subject><subject>RNA</subject><subject>Soybeans</subject><subject>Transcription, Genetic</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhi0EokvhjoQEFgfEJYu_4sSIS1WgVFrgQDlbXsfZeuW1UztG5c4Px9ks0HKA00gzz_vO2DMAPMZoiVFDXw1epaXgS8KWmLac3gELjASuOBPoLlggRJqqZYQdgQcpbRFCom7RfXCEUd0gzNkC_Dj3Y1TaOJedivDMeAMvovKpNxFaD0_0aIN_Dd9m5eaCjnaYclD5Dn7MbrSDM_CLdcZr6zcJhh5-ytqZYrdH7Bj0ZfBdtMVCh2uy75Im95XZ5J1JD8G9XrlkHh3iMfj6_t3F6Ydq9fns_PRkVema1GMlcCdM0ytBcQlUtGu1bkhrWM_WTVNzreqSVTUmQvQUc4wIUxR3LW9Z17eYHoM3s--Q1zvTaTO93ckh2p2K32VQVt6ueHspN-GbJAzXvMhfHOQxXGWTRrmzafo65U3ISXJBEWME_RfEDUMNpnUBn_8FbkOOvvyBJKhsFDFBC4RmSMeQUjT974ExktMZyOkMpOBlTLk_gyJ5evOhNwTz3gvw7ABM0l_l2xYv_03IPjs3muuxoE9mdJvGEP80I5hiSn8CN_XRZA</recordid><startdate>19991123</startdate><enddate>19991123</enddate><creator>Adams, Keith L.</creator><creator>Song, Keming</creator><creator>Roessler, Philip G.</creator><creator>Nugent, Jacqueline M.</creator><creator>Doyle, Jane L.</creator><creator>Doyle, Jeff J.</creator><creator>Palmer, Jeffrey D.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19991123</creationdate><title>Intracellular Gene Transfer in Action: Dual Transcription and Multiple Silencings of Nuclear and Mitochondrial cox2 Genes in Legumes</title><author>Adams, Keith L. ; Song, Keming ; Roessler, Philip G. ; Nugent, Jacqueline M. ; Doyle, Jane L. ; Doyle, Jeff J. ; Palmer, Jeffrey D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-91d9e7fa931e7f398bab728e4f4b7756ca5f39a51299f3161024a31d8684df813</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1999</creationdate><topic>Biological Sciences</topic><topic>Botany</topic><topic>Cell Nucleus</topic><topic>Complementary DNA</topic><topic>cox2 gene</topic><topic>DNA</topic><topic>Electron Transport Complex IV - genetics</topic><topic>Evolution</topic><topic>Fabaceae - enzymology</topic><topic>Fabaceae - genetics</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Genetic hybridization</topic><topic>Genomes</topic><topic>Legumes</topic><topic>Leguminosae</topic><topic>Mitochondria - genetics</topic><topic>Molecular Sequence Data</topic><topic>Plant Proteins - genetics</topic><topic>Plants, Medicinal</topic><topic>Recombination, Genetic</topic><topic>Reverse transcriptase polymerase chain reaction</topic><topic>RNA</topic><topic>Soybeans</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Adams, Keith L.</creatorcontrib><creatorcontrib>Song, Keming</creatorcontrib><creatorcontrib>Roessler, Philip G.</creatorcontrib><creatorcontrib>Nugent, Jacqueline M.</creatorcontrib><creatorcontrib>Doyle, Jane L.</creatorcontrib><creatorcontrib>Doyle, Jeff J.</creatorcontrib><creatorcontrib>Palmer, Jeffrey D.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Adams, Keith L.</au><au>Song, Keming</au><au>Roessler, Philip G.</au><au>Nugent, Jacqueline M.</au><au>Doyle, Jane L.</au><au>Doyle, Jeff J.</au><au>Palmer, Jeffrey D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Intracellular Gene Transfer in Action: Dual Transcription and Multiple Silencings of Nuclear and Mitochondrial cox2 Genes in Legumes</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>1999-11-23</date><risdate>1999</risdate><volume>96</volume><issue>24</issue><spage>13863</spage><epage>13868</epage><pages>13863-13868</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The respiratory gene cox2, normally present in the mitochondrion, was previously shown to have been functionally transferred to the nucleus during flowering plant evolution, possibly during the diversification of legumes. To search for novel intermediate stages in the process of intracellular gene transfer and to assess the evolutionary timing and frequency of cox2 transfer, activation, and inactivation, we examined nuclear and mitochondrial (mt) cox2 presence and expression in over 25 legume genera and mt cox2 presence in 392 genera. Transfer and activation of cox2 appear to have occurred during recent legume evolution, more recently than previously inferred. Many intermediate stages of the gene transfer process are represented by cox2 genes in the studied legumes. Nine legumes contain intact copies of both nuclear and mt cox2, although transcripts could not be detected for some of these genes. Both cox2 genes are transcribed in seven legumes that are phylogenetically interspersed with species displaying only nuclear or mt cox2 expression. Inactivation of cox2 in each genome has taken place multiple times and in a variety of ways, including loss of detectable transcripts or transcript editing and partial to complete gene loss. Phylogenetic evidence shows about the same number (3-5) of separate inactivations of nuclear and mt cox2, suggesting that there is no selective advantage for a mt vs. nuclear location of cox2 in plants. The current distribution of cox2 presence and expression between the nucleus and mitochondrion in the studied legumes is probably the result of chance mutations silencing either cox2 gene.</abstract><cop>United States</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>10570164</pmid><doi>10.1073/pnas.96.24.13863</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Biological Sciences Botany Cell Nucleus Complementary DNA cox2 gene DNA Electron Transport Complex IV - genetics Evolution Fabaceae - enzymology Fabaceae - genetics Genes Genes, Plant Genetic hybridization Genomes Legumes Leguminosae Mitochondria - genetics Molecular Sequence Data Plant Proteins - genetics Plants, Medicinal Recombination, Genetic Reverse transcriptase polymerase chain reaction RNA Soybeans Transcription, Genetic |
title | Intracellular Gene Transfer in Action: Dual Transcription and Multiple Silencings of Nuclear and Mitochondrial cox2 Genes in Legumes |
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