Diversified regulation of circadian clock gene expression following whole genome duplication
Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple co...
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description | Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes. |
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In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1009097</identifier><identifier>PMID: 33031398</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anadromous species ; Animals ; Biology and Life Sciences ; Brain research ; Chromosomes ; Circadian Clocks - genetics ; Circadian rhythm ; Circadian rhythms ; Clock gene ; Cortisol ; Divergence ; Evolution, Molecular ; Gene Duplication - genetics ; Gene expression ; Gene Expression Regulation, Developmental - genetics ; Gene Regulatory Networks - genetics ; Genetic aspects ; Genetic regulation ; Genetic research ; Genome - genetics ; Genomes ; Life sciences ; Mammals ; Marine biology ; Matematikk og Naturvitenskap: 400 ; Mathematics and natural science: 400 ; Medicine and Health Sciences ; Metabolism ; Oscillations ; Phylogenetics ; Phylogeny ; Physiology ; Proteins ; Salmo salar ; Salmo salar - genetics ; Transcription ; VDP ; Vertebrates ; Zebrafish ; Zoologiske og botaniske fag: 480 ; Zoology and botany: 480</subject><ispartof>PLoS genetics, 2020-10, Vol.16 (10), p.e1009097</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 West 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. 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In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. 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genetics</subject><subject>Transcription</subject><subject>VDP</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><subject>Zoologiske og botaniske fag: 480</subject><subject>Zoology and botany: 480</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</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>3HK</sourceid><sourceid>DOA</sourceid><recordid>eNqVk1uLEzEUgAdR3HX1H4gOCIIPrUmTTCYvwrKuWlhc8PYkhDQ5maamk5rM7OXfm-5O1w4oKIEknHznnlMUTzGaYsLx61XoY6v8dNNAO8UICST4veIQM0YmnCJ6f-9-UDxKaYUQYbXgD4sDQhDBRNSHxfe37gJictaBKSM0vVedC20ZbKld1Mo41ZbaB_2jzH6ghKtNhJS2iA3eh0vXNuXlMnjYvoc1lKbfeKdvrDwuHljlEzwZzqPi67vTLycfJmfn7-cnx2cTzRnqJqQShHMEBGyNK4uogboSqqqINUwsmNBqBoLVmJHaYktAGGWUXRAOnBpmyVHx_Nbuxockh8IkOaMVwhgjITIxvyVMUCu5iW6t4rUMyskbQYiNVLFz2oNEHMPMMG4oFbQCVVuDZkKJmjMKCuNs683grV-swWhou6j8yOj4pXVL2YQLyVlOt-a_w9XRpc61sg1RydxCwuUsbyQTLwYXMfzsIXV_SWqgGpXjdq0N2Z1eu6TlcUUZIVQIlqnpH6i8DKydDi1Yl-UjhVcjhcx0cNU1qk9Jzj9_-g_247-z59_G7Ms9dgnKd8sUfL_9VWkM0l0tQ0oR7F0fMJLbOdlVTm7nRA5zktWe7ffwTmk3GOQXLdkMOg</recordid><startdate>20201008</startdate><enddate>20201008</enddate><creator>West, Alexander C</creator><creator>Iversen, Marianne</creator><creator>Jørgensen, Even H</creator><creator>Sandve, Simen R</creator><creator>Hazlerigg, David G</creator><creator>Wood, Shona H</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</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>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>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>3HK</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-8273-4045</orcidid><orcidid>https://orcid.org/0000-0003-4884-8409</orcidid><orcidid>https://orcid.org/0000-0003-1020-4018</orcidid><orcidid>https://orcid.org/0000-0003-3934-5068</orcidid></search><sort><creationdate>20201008</creationdate><title>Diversified regulation of circadian clock gene expression following whole genome duplication</title><author>West, Alexander C ; Iversen, Marianne ; Jørgensen, Even H ; Sandve, Simen R ; Hazlerigg, David G ; Wood, Shona H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c750t-3693770e3ef816f04de869a663fd59b59ca2e9581538f1f3e9dadafb37e74d5f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Anadromous species</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Brain research</topic><topic>Chromosomes</topic><topic>Circadian Clocks - 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Norwegian Open Research Archives</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>West, Alexander C</au><au>Iversen, Marianne</au><au>Jørgensen, Even H</au><au>Sandve, Simen R</au><au>Hazlerigg, David G</au><au>Wood, Shona H</au><au>Ewer, John</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diversified regulation of circadian clock gene expression following whole genome duplication</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2020-10-08</date><risdate>2020</risdate><volume>16</volume><issue>10</issue><spage>e1009097</spage><pages>e1009097-</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called 'clock genes', collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene- and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh- to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33031398</pmid><doi>10.1371/journal.pgen.1009097</doi><orcidid>https://orcid.org/0000-0002-8273-4045</orcidid><orcidid>https://orcid.org/0000-0003-4884-8409</orcidid><orcidid>https://orcid.org/0000-0003-1020-4018</orcidid><orcidid>https://orcid.org/0000-0003-3934-5068</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anadromous species Animals Biology and Life Sciences Brain research Chromosomes Circadian Clocks - genetics Circadian rhythm Circadian rhythms Clock gene Cortisol Divergence Evolution, Molecular Gene Duplication - genetics Gene expression Gene Expression Regulation, Developmental - genetics Gene Regulatory Networks - genetics Genetic aspects Genetic regulation Genetic research Genome - genetics Genomes Life sciences Mammals Marine biology Matematikk og Naturvitenskap: 400 Mathematics and natural science: 400 Medicine and Health Sciences Metabolism Oscillations Phylogenetics Phylogeny Physiology Proteins Salmo salar Salmo salar - genetics Transcription VDP Vertebrates Zebrafish Zoologiske og botaniske fag: 480 Zoology and botany: 480 |
title | Diversified regulation of circadian clock gene expression following whole genome duplication |
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