Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes
Whole-genome duplication events (polyploidy events) and gene loss events have played important roles in the evolution of legumes. Here we show that the vast majority of Hsf gene duplications resulted from whole genome duplication events rather than tandem duplication, and significant differences in...
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| description | Whole-genome duplication events (polyploidy events) and gene loss events have played important roles in the evolution of legumes. Here we show that the vast majority of Hsf gene duplications resulted from whole genome duplication events rather than tandem duplication, and significant differences in gene retention exist between species. By searching for intraspecies gene colinearity (microsynteny) and dating the age distributions of duplicated genes, we found that genome duplications accounted for 42 of 46 Hsf-containing segments in Glycine max, while paired segments were rarely identified in Lotus japonicas, Medicago truncatula and Cajanus cajan. However, by comparing interspecies microsynteny, we determined that the great majority of Hsf-containing segments in Lotus japonicas, Medicago truncatula and Cajanus cajan show extensive conservation with the duplicated regions of Glycine max. These segments formed 17 groups of orthologous segments. These results suggest that these regions shared ancient genome duplication with Hsf genes in Glycine max, but more than half of the copies of these genes were lost. On the other hand, the Glycine max Hsf gene family retained approximately 75% and 84% of duplicated genes produced from the ancient genome duplication and recent Glycine-specific genome duplication, respectively. Continuous purifying selection has played a key role in the maintenance of Hsf genes in Glycine max. Expression analysis of the Hsf genes in Lotus japonicus revealed their putative involvement in multiple tissue-/developmental stages and responses to various abiotic stimuli. This study traces the evolution of Hsf genes in legume species and demonstrates that the rates of gene gain and loss are far from equilibrium in different species. |
| doi_str_mv | 10.1371/journal.pone.0102825 |
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Here we show that the vast majority of Hsf gene duplications resulted from whole genome duplication events rather than tandem duplication, and significant differences in gene retention exist between species. By searching for intraspecies gene colinearity (microsynteny) and dating the age distributions of duplicated genes, we found that genome duplications accounted for 42 of 46 Hsf-containing segments in Glycine max, while paired segments were rarely identified in Lotus japonicas, Medicago truncatula and Cajanus cajan. However, by comparing interspecies microsynteny, we determined that the great majority of Hsf-containing segments in Lotus japonicas, Medicago truncatula and Cajanus cajan show extensive conservation with the duplicated regions of Glycine max. These segments formed 17 groups of orthologous segments. These results suggest that these regions shared ancient genome duplication with Hsf genes in Glycine max, but more than half of the copies of these genes were lost. On the other hand, the Glycine max Hsf gene family retained approximately 75% and 84% of duplicated genes produced from the ancient genome duplication and recent Glycine-specific genome duplication, respectively. Continuous purifying selection has played a key role in the maintenance of Hsf genes in Glycine max. Expression analysis of the Hsf genes in Lotus japonicus revealed their putative involvement in multiple tissue-/developmental stages and responses to various abiotic stimuli. This study traces the evolution of Hsf genes in legume species and demonstrates that the rates of gene gain and loss are far from equilibrium in different species.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0102825</identifier><identifier>PMID: 25047803</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alfalfa ; Arabidopsis ; Biological evolution ; Biology ; Biology and Life Sciences ; Cajanus - genetics ; Cajanus cajan ; Conservation ; Dating techniques ; Developmental stages ; DNA-Binding Proteins - genetics ; Evolution ; Evolution, Molecular ; Evolutionary genetics ; Fabaceae - genetics ; Gene amplification ; Gene Duplication ; Gene expression ; Genes ; Genes, Plant ; Genome, Plant ; Genomes ; Genomics ; Glycine max - genetics ; Heat ; Heat shock ; Heat shock factors ; Heat shock proteins ; Heat Shock Transcription Factors ; Legumes ; Life sciences ; Lotus - genetics ; Medicago truncatula - genetics ; Oryza ; Physiology ; Polyploidy ; Reproduction (copying) ; Research and Analysis Methods ; Segments ; Signal transduction ; Species ; Stress response ; Transcription factors ; Transcription Factors - genetics</subject><ispartof>PloS one, 2014-07, Vol.9 (7), p.e102825</ispartof><rights>2014 Lin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Lin et al 2014 Lin et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-30051a61ad557cc5568962c2d9072351dfa23fd2f56cf1bb8910726f7846d21b3</citedby><cites>FETCH-LOGICAL-c526t-30051a61ad557cc5568962c2d9072351dfa23fd2f56cf1bb8910726f7846d21b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4105503/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4105503/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25047803$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Robinson-Rechavi, Marc</contributor><creatorcontrib>Lin, Yongxiang</creatorcontrib><creatorcontrib>Cheng, Ying</creatorcontrib><creatorcontrib>Jin, Jing</creatorcontrib><creatorcontrib>Jin, Xiaolei</creatorcontrib><creatorcontrib>Jiang, Haiyang</creatorcontrib><creatorcontrib>Yan, Hanwei</creatorcontrib><creatorcontrib>Cheng, Beijiu</creatorcontrib><title>Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Whole-genome duplication events (polyploidy events) and gene loss events have played important roles in the evolution of legumes. Here we show that the vast majority of Hsf gene duplications resulted from whole genome duplication events rather than tandem duplication, and significant differences in gene retention exist between species. By searching for intraspecies gene colinearity (microsynteny) and dating the age distributions of duplicated genes, we found that genome duplications accounted for 42 of 46 Hsf-containing segments in Glycine max, while paired segments were rarely identified in Lotus japonicas, Medicago truncatula and Cajanus cajan. However, by comparing interspecies microsynteny, we determined that the great majority of Hsf-containing segments in Lotus japonicas, Medicago truncatula and Cajanus cajan show extensive conservation with the duplicated regions of Glycine max. These segments formed 17 groups of orthologous segments. These results suggest that these regions shared ancient genome duplication with Hsf genes in Glycine max, but more than half of the copies of these genes were lost. On the other hand, the Glycine max Hsf gene family retained approximately 75% and 84% of duplicated genes produced from the ancient genome duplication and recent Glycine-specific genome duplication, respectively. Continuous purifying selection has played a key role in the maintenance of Hsf genes in Glycine max. Expression analysis of the Hsf genes in Lotus japonicus revealed their putative involvement in multiple tissue-/developmental stages and responses to various abiotic stimuli. This study traces the evolution of Hsf genes in legume species and demonstrates that the rates of gene gain and loss are far from equilibrium in different species.</description><subject>Alfalfa</subject><subject>Arabidopsis</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cajanus - genetics</subject><subject>Cajanus cajan</subject><subject>Conservation</subject><subject>Dating techniques</subject><subject>Developmental stages</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary genetics</subject><subject>Fabaceae - genetics</subject><subject>Gene amplification</subject><subject>Gene Duplication</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genome, Plant</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glycine max - genetics</subject><subject>Heat</subject><subject>Heat shock</subject><subject>Heat shock factors</subject><subject>Heat shock proteins</subject><subject>Heat Shock Transcription Factors</subject><subject>Legumes</subject><subject>Life sciences</subject><subject>Lotus - genetics</subject><subject>Medicago truncatula - genetics</subject><subject>Oryza</subject><subject>Physiology</subject><subject>Polyploidy</subject><subject>Reproduction (copying)</subject><subject>Research and Analysis Methods</subject><subject>Segments</subject><subject>Signal transduction</subject><subject>Species</subject><subject>Stress response</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</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><sourceid>DOA</sourceid><recordid>eNptUk1v1DAUjBCIlsI_QGCJC5dd_BE7zgWpqqBUqsQFzpZjP-96cexgJ5X492SzadUiTrY88-bNe56qekvwlrCGfDqkKUcdtkOKsMUEU0n5s-qctIxuBMXs-aP7WfWqlAPGnEkhXlZnlOO6kZidV_4aYuoB2WkI3ujRp4h0tGgHEVBIpSDtHJgRjXtAcJfCtFCSQ3vQIyr7ZH6hMetYTPbDgjltxpQXhYJ8RAF2Uw_ldfXC6VDgzXpeVD-_fvlx9W1z-_365urydmM4FeOGzS6JFkRbzhtjOBeyFdRQ2-KGMk6s05Q5Sx0XxpGuky2ZAeEaWQtLSccuqvcn3WG2r9YtFUV43TAs66adGTcnhk36oIbse53_qKS9Wh5S3imdR28CKOksY7qzjDZt3Zp5fU4KYBrblnQW01nr89pt6nqwBuK8jPBE9CkS_V7t0p2qCeYcs1ng4yqQ0-8Jyqh6XwyEoCOkafEtBaOCH3t9-If6_-nqE8vk-fsyuAczBKtjcu6r1DE5ak3OXPbu8SAPRfdRYX8BBDXCIg</recordid><startdate>20140721</startdate><enddate>20140721</enddate><creator>Lin, Yongxiang</creator><creator>Cheng, Ying</creator><creator>Jin, Jing</creator><creator>Jin, Xiaolei</creator><creator>Jiang, Haiyang</creator><creator>Yan, Hanwei</creator><creator>Cheng, Beijiu</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140721</creationdate><title>Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes</title><author>Lin, Yongxiang ; Cheng, Ying ; Jin, Jing ; Jin, Xiaolei ; Jiang, Haiyang ; Yan, Hanwei ; Cheng, Beijiu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-30051a61ad557cc5568962c2d9072351dfa23fd2f56cf1bb8910726f7846d21b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Alfalfa</topic><topic>Arabidopsis</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cajanus - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Yongxiang</au><au>Cheng, Ying</au><au>Jin, Jing</au><au>Jin, Xiaolei</au><au>Jiang, Haiyang</au><au>Yan, Hanwei</au><au>Cheng, Beijiu</au><au>Robinson-Rechavi, Marc</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-07-21</date><risdate>2014</risdate><volume>9</volume><issue>7</issue><spage>e102825</spage><pages>e102825-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Whole-genome duplication events (polyploidy events) and gene loss events have played important roles in the evolution of legumes. Here we show that the vast majority of Hsf gene duplications resulted from whole genome duplication events rather than tandem duplication, and significant differences in gene retention exist between species. By searching for intraspecies gene colinearity (microsynteny) and dating the age distributions of duplicated genes, we found that genome duplications accounted for 42 of 46 Hsf-containing segments in Glycine max, while paired segments were rarely identified in Lotus japonicas, Medicago truncatula and Cajanus cajan. However, by comparing interspecies microsynteny, we determined that the great majority of Hsf-containing segments in Lotus japonicas, Medicago truncatula and Cajanus cajan show extensive conservation with the duplicated regions of Glycine max. These segments formed 17 groups of orthologous segments. These results suggest that these regions shared ancient genome duplication with Hsf genes in Glycine max, but more than half of the copies of these genes were lost. On the other hand, the Glycine max Hsf gene family retained approximately 75% and 84% of duplicated genes produced from the ancient genome duplication and recent Glycine-specific genome duplication, respectively. Continuous purifying selection has played a key role in the maintenance of Hsf genes in Glycine max. Expression analysis of the Hsf genes in Lotus japonicus revealed their putative involvement in multiple tissue-/developmental stages and responses to various abiotic stimuli. This study traces the evolution of Hsf genes in legume species and demonstrates that the rates of gene gain and loss are far from equilibrium in different species.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25047803</pmid><doi>10.1371/journal.pone.0102825</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Alfalfa Arabidopsis Biological evolution Biology Biology and Life Sciences Cajanus - genetics Cajanus cajan Conservation Dating techniques Developmental stages DNA-Binding Proteins - genetics Evolution Evolution, Molecular Evolutionary genetics Fabaceae - genetics Gene amplification Gene Duplication Gene expression Genes Genes, Plant Genome, Plant Genomes Genomics Glycine max - genetics Heat Heat shock Heat shock factors Heat shock proteins Heat Shock Transcription Factors Legumes Life sciences Lotus - genetics Medicago truncatula - genetics Oryza Physiology Polyploidy Reproduction (copying) Research and Analysis Methods Segments Signal transduction Species Stress response Transcription factors Transcription Factors - genetics |
| title | Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes |
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