Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth
Summary Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem d...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2007-06, Vol.50 (5), p.873-885 |
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creator | Kong, Hongzhi Landherr, Lena L. Frohlich, Michael W. Leebens‐Mack, Jim Ma, Hong DePamphilis, Claude W. |
description | Summary
Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem duplication and retroposition. Although segmental and tandem duplications have been found to be important for the expansion of a number of multigene families, the contribution of retroposition is not clear. Here we show that plant SKP1 genes have evolved by multiple duplication events from a single ancestral copy in the most recent common ancestor (MRCA) of eudicots and monocots, resulting in 19 ASK (Arabidopsis SKP1‐like) and 28 OSK (Oryza SKP1‐like) genes. The estimated birth rates are more than ten times the average rate of gene duplication, and are even higher than that of other rapidly duplicating plant genes, such as type I MADS box genes, R genes, and genes encoding receptor‐like kinases. Further analyses suggest that a relatively large proportion of the duplication events may be explained by tandem duplication, but few, if any, are likely to be due to segmental duplication. In addition, by mapping the gain/loss of a specific intron on gene phylogenies, and by searching for the features that characterize retrogenes/retrosequences, we show that retroposition is an important mechanism for expansion of the plant SKP1 gene family. Specifically, we propose that two and three ancient retroposition events occurred in lineages leading to Arabidopsis and rice, respectively, followed by repeated tandem duplications and chromosome rearrangements. Our study represents a thorough investigation showing that retroposition can play an important role in the evolution of a plant gene family whose members do not encode mobile elements. |
doi_str_mv | 10.1111/j.1365-313X.2007.03097.x |
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Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem duplication and retroposition. Although segmental and tandem duplications have been found to be important for the expansion of a number of multigene families, the contribution of retroposition is not clear. Here we show that plant SKP1 genes have evolved by multiple duplication events from a single ancestral copy in the most recent common ancestor (MRCA) of eudicots and monocots, resulting in 19 ASK (Arabidopsis SKP1‐like) and 28 OSK (Oryza SKP1‐like) genes. The estimated birth rates are more than ten times the average rate of gene duplication, and are even higher than that of other rapidly duplicating plant genes, such as type I MADS box genes, R genes, and genes encoding receptor‐like kinases. Further analyses suggest that a relatively large proportion of the duplication events may be explained by tandem duplication, but few, if any, are likely to be due to segmental duplication. In addition, by mapping the gain/loss of a specific intron on gene phylogenies, and by searching for the features that characterize retrogenes/retrosequences, we show that retroposition is an important mechanism for expansion of the plant SKP1 gene family. Specifically, we propose that two and three ancient retroposition events occurred in lineages leading to Arabidopsis and rice, respectively, followed by repeated tandem duplications and chromosome rearrangements. Our study represents a thorough investigation showing that retroposition can play an important role in the evolution of a plant gene family whose members do not encode mobile elements.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/j.1365-313X.2007.03097.x</identifier><identifier>PMID: 17470057</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - classification ; Arabidopsis - genetics ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Base Sequence ; Biological and medical sciences ; birth‐and‐death evolution ; Botany ; Evolutionary biology ; Fundamental and applied biological sciences. Psychology ; Gene Duplication ; Genes ; Genes. Genome ; Molecular and cellular biology ; Molecular genetics ; Molecular Sequence Data ; Multigene Family ; Oryza ; Oryza - classification ; Oryza - genetics ; Oryza sativa ; Phylogeny ; plant SKP1 genes ; Reproduction ; retroposition ; S-Phase Kinase-Associated Proteins - genetics ; S-Phase Kinase-Associated Proteins - metabolism ; segmental duplication ; tandem duplication</subject><ispartof>The Plant journal : for cell and molecular biology, 2007-06, Vol.50 (5), p.873-885</ispartof><rights>2007 INIST-CNRS</rights><rights>2007 The Authors Journal compilation 2007 Blackwell Publishing Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5767-71a51026baa16835644102847239bd96b34aa57c244d360412f089103ec02efa3</citedby><cites>FETCH-LOGICAL-c5767-71a51026baa16835644102847239bd96b34aa57c244d360412f089103ec02efa3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-313X.2007.03097.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-313X.2007.03097.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18794397$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17470057$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kong, Hongzhi</creatorcontrib><creatorcontrib>Landherr, Lena L.</creatorcontrib><creatorcontrib>Frohlich, Michael W.</creatorcontrib><creatorcontrib>Leebens‐Mack, Jim</creatorcontrib><creatorcontrib>Ma, Hong</creatorcontrib><creatorcontrib>DePamphilis, Claude W.</creatorcontrib><title>Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem duplication and retroposition. Although segmental and tandem duplications have been found to be important for the expansion of a number of multigene families, the contribution of retroposition is not clear. Here we show that plant SKP1 genes have evolved by multiple duplication events from a single ancestral copy in the most recent common ancestor (MRCA) of eudicots and monocots, resulting in 19 ASK (Arabidopsis SKP1‐like) and 28 OSK (Oryza SKP1‐like) genes. The estimated birth rates are more than ten times the average rate of gene duplication, and are even higher than that of other rapidly duplicating plant genes, such as type I MADS box genes, R genes, and genes encoding receptor‐like kinases. Further analyses suggest that a relatively large proportion of the duplication events may be explained by tandem duplication, but few, if any, are likely to be due to segmental duplication. In addition, by mapping the gain/loss of a specific intron on gene phylogenies, and by searching for the features that characterize retrogenes/retrosequences, we show that retroposition is an important mechanism for expansion of the plant SKP1 gene family. Specifically, we propose that two and three ancient retroposition events occurred in lineages leading to Arabidopsis and rice, respectively, followed by repeated tandem duplications and chromosome rearrangements. Our study represents a thorough investigation showing that retroposition can play an important role in the evolution of a plant gene family whose members do not encode mobile elements.</description><subject>Arabidopsis</subject><subject>Arabidopsis - classification</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Base Sequence</subject><subject>Biological and medical sciences</subject><subject>birth‐and‐death evolution</subject><subject>Botany</subject><subject>Evolutionary biology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Duplication</subject><subject>Genes</subject><subject>Genes. Genome</subject><subject>Molecular and cellular biology</subject><subject>Molecular genetics</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Oryza</subject><subject>Oryza - classification</subject><subject>Oryza - genetics</subject><subject>Oryza sativa</subject><subject>Phylogeny</subject><subject>plant SKP1 genes</subject><subject>Reproduction</subject><subject>retroposition</subject><subject>S-Phase Kinase-Associated Proteins - genetics</subject><subject>S-Phase Kinase-Associated Proteins - metabolism</subject><subject>segmental duplication</subject><subject>tandem duplication</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU-L1TAUxYMoznP0K0gQdNd606RJK7iQwfHfgA8cwV1I03ReHmnaSVpn3sqvbjp9OOBGs0ku93fPzeEghAnkJJ3X-5xQXmaU0B95ASByoFCL_PYB2vxpPEQbqDlkgpHiBD2JcQ9ABOXsMTohggmAUmzQr62aJhN8xEOHr4w3uJ1HZ7Wa7OCx9XjaGTw65Sf87cuWrEineusOS1f5KzvE0YQ-vsHmp22N16k_BNzPbrKjM7g3eqe8jf3diqBG264qjQ3T7il61CkXzbPjfYq-n7-_PPuYXXz98Ons3UWmS8FFJogqCRS8UYrwipacsVRWTBS0btqaN5QpVQpdMNZSDslyB1VNgBoNhekUPUWvVt0xDNeziZPsbdTGJWdmmKMUUNaCk-KfYAElSWurBL74C9wPc_DJhCwIZVARRhJUrZAOQ4zBdHIMtlfhIAnIJUq5l0ticklMLlHKuyjlbRp9ftSfm96094PH7BLw8gioqJXrgvLaxnuuEjWj9cK9Xbkb68zhvz8gL7eflxf9DWG5uL8</recordid><startdate>200706</startdate><enddate>200706</enddate><creator>Kong, Hongzhi</creator><creator>Landherr, Lena L.</creator><creator>Frohlich, Michael W.</creator><creator>Leebens‐Mack, Jim</creator><creator>Ma, Hong</creator><creator>DePamphilis, Claude W.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell Science</general><scope>IQODW</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>200706</creationdate><title>Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth</title><author>Kong, Hongzhi ; Landherr, Lena L. ; Frohlich, Michael W. ; Leebens‐Mack, Jim ; Ma, Hong ; DePamphilis, Claude W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5767-71a51026baa16835644102847239bd96b34aa57c244d360412f089103ec02efa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - classification</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Base Sequence</topic><topic>Biological and medical sciences</topic><topic>birth‐and‐death evolution</topic><topic>Botany</topic><topic>Evolutionary biology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Duplication</topic><topic>Genes</topic><topic>Genes. Genome</topic><topic>Molecular and cellular biology</topic><topic>Molecular genetics</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family</topic><topic>Oryza</topic><topic>Oryza - classification</topic><topic>Oryza - genetics</topic><topic>Oryza sativa</topic><topic>Phylogeny</topic><topic>plant SKP1 genes</topic><topic>Reproduction</topic><topic>retroposition</topic><topic>S-Phase Kinase-Associated Proteins - genetics</topic><topic>S-Phase Kinase-Associated Proteins - metabolism</topic><topic>segmental duplication</topic><topic>tandem duplication</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kong, Hongzhi</creatorcontrib><creatorcontrib>Landherr, Lena L.</creatorcontrib><creatorcontrib>Frohlich, Michael W.</creatorcontrib><creatorcontrib>Leebens‐Mack, Jim</creatorcontrib><creatorcontrib>Ma, Hong</creatorcontrib><creatorcontrib>DePamphilis, Claude W.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kong, Hongzhi</au><au>Landherr, Lena L.</au><au>Frohlich, Michael W.</au><au>Leebens‐Mack, Jim</au><au>Ma, Hong</au><au>DePamphilis, Claude W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2007-06</date><risdate>2007</risdate><volume>50</volume><issue>5</issue><spage>873</spage><epage>885</epage><pages>873-885</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem duplication and retroposition. Although segmental and tandem duplications have been found to be important for the expansion of a number of multigene families, the contribution of retroposition is not clear. Here we show that plant SKP1 genes have evolved by multiple duplication events from a single ancestral copy in the most recent common ancestor (MRCA) of eudicots and monocots, resulting in 19 ASK (Arabidopsis SKP1‐like) and 28 OSK (Oryza SKP1‐like) genes. The estimated birth rates are more than ten times the average rate of gene duplication, and are even higher than that of other rapidly duplicating plant genes, such as type I MADS box genes, R genes, and genes encoding receptor‐like kinases. Further analyses suggest that a relatively large proportion of the duplication events may be explained by tandem duplication, but few, if any, are likely to be due to segmental duplication. In addition, by mapping the gain/loss of a specific intron on gene phylogenies, and by searching for the features that characterize retrogenes/retrosequences, we show that retroposition is an important mechanism for expansion of the plant SKP1 gene family. Specifically, we propose that two and three ancient retroposition events occurred in lineages leading to Arabidopsis and rice, respectively, followed by repeated tandem duplications and chromosome rearrangements. Our study represents a thorough investigation showing that retroposition can play an important role in the evolution of a plant gene family whose members do not encode mobile elements.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>17470057</pmid><doi>10.1111/j.1365-313X.2007.03097.x</doi><tpages>13</tpages></addata></record> |
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subjects | Arabidopsis Arabidopsis - classification Arabidopsis - genetics Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Base Sequence Biological and medical sciences birth‐and‐death evolution Botany Evolutionary biology Fundamental and applied biological sciences. Psychology Gene Duplication Genes Genes. Genome Molecular and cellular biology Molecular genetics Molecular Sequence Data Multigene Family Oryza Oryza - classification Oryza - genetics Oryza sativa Phylogeny plant SKP1 genes Reproduction retroposition S-Phase Kinase-Associated Proteins - genetics S-Phase Kinase-Associated Proteins - metabolism segmental duplication tandem duplication |
title | Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth |
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