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
Hauptverfasser: Kong, Hongzhi, Landherr, Lena L., Frohlich, Michael W., Leebens‐Mack, Jim, Ma, Hong, DePamphilis, Claude W.
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container_issue 5
container_start_page 873
container_title The Plant journal : for cell and molecular biology
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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 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. 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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. 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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. 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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. 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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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