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The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi
Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden e...
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Published in: | PLoS genetics 2017-07, Vol.13 (7), p.e1006867-e1006867 |
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description | Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development. |
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To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006867</identifier><identifier>PMID: 28704372</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bayes Theorem ; Bayesian analysis ; Bioinformatics ; Biological Evolution ; Biology and Life Sciences ; Computer and Information Sciences ; Consortia ; Developmental biology ; Developmental stages ; Divergence ; Evolution ; Evolutionary biology ; Fruit bodies ; Fruiting Bodies, Fungal - genetics ; Funding ; Fungi ; Fungi - genetics ; Gene deletion ; Gene expression ; Gene Expression Regulation, Fungal - genetics ; Gene families ; Gene Knockout Techniques ; Genetic aspects ; Genome, Fungal - genetics ; Genomes ; Genomics ; Medicine and Health Sciences ; Molds (Fungi) ; Morphology ; Neurospora crassa - genetics ; Observations ; Phenotype ; Phenotypes ; Phylogenetics ; Phylogeny ; Plant biology ; Quality control ; Research and Analysis Methods ; Roles ; Sex Differentiation - genetics ; Sordariales - genetics ; Sordariales - growth & development ; Transcription ; Transcription (Genetics) ; Transcriptome - genetics</subject><ispartof>PLoS genetics, 2017-07, Vol.13 (7), p.e1006867-e1006867</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Trail F, Wang Z, Stefanko K, Cubba C, Townsend JP (2017) The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi. PLoS Genet 13(7): e1006867. https://doi.org/10.1371/journal.pgen.1006867</rights><rights>2017 Trail et al 2017 Trail et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Trail F, Wang Z, Stefanko K, Cubba C, Townsend JP (2017) The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi. PLoS Genet 13(7): e1006867. https://doi.org/10.1371/journal.pgen.1006867</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-42fe777ed3ad660fbc21ff47ceac45c3f86586e33fcf1db2a489f1eed6423b13</citedby><cites>FETCH-LOGICAL-c726t-42fe777ed3ad660fbc21ff47ceac45c3f86586e33fcf1db2a489f1eed6423b13</cites><orcidid>0000-0002-9890-3907</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1929401764/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1929401764?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28704372$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Fraser, Hunter B.</contributor><creatorcontrib>Trail, Frances</creatorcontrib><creatorcontrib>Wang, Zheng</creatorcontrib><creatorcontrib>Stefanko, Kayla</creatorcontrib><creatorcontrib>Cubba, Caitlyn</creatorcontrib><creatorcontrib>Townsend, Jeffrey P</creatorcontrib><title>The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development.</description><subject>Bayes Theorem</subject><subject>Bayesian analysis</subject><subject>Bioinformatics</subject><subject>Biological Evolution</subject><subject>Biology and Life Sciences</subject><subject>Computer and Information Sciences</subject><subject>Consortia</subject><subject>Developmental biology</subject><subject>Developmental stages</subject><subject>Divergence</subject><subject>Evolution</subject><subject>Evolutionary biology</subject><subject>Fruit bodies</subject><subject>Fruiting Bodies, Fungal - genetics</subject><subject>Funding</subject><subject>Fungi</subject><subject>Fungi - genetics</subject><subject>Gene deletion</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Fungal - genetics</subject><subject>Gene families</subject><subject>Gene Knockout Techniques</subject><subject>Genetic aspects</subject><subject>Genome, Fungal - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Medicine and Health Sciences</subject><subject>Molds (Fungi)</subject><subject>Morphology</subject><subject>Neurospora crassa - genetics</subject><subject>Observations</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant biology</subject><subject>Quality control</subject><subject>Research and Analysis Methods</subject><subject>Roles</subject><subject>Sex Differentiation - genetics</subject><subject>Sordariales - genetics</subject><subject>Sordariales - growth & development</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Transcriptome - genetics</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11v0zAUhiMEYmPwDxBEQkJw0WLHX8kN0jTxUWliElTcWq5znLpy7SxOqu3f467Z1KBdgHKR2Hne1znvycmy1xjNMRH40yYMnVdu3jbg5xghXnLxJDvFjJGZoIg-PXo-yV7EuEGIsLISz7OTohSIElGcZmq5hlx5DbHvlMsd7MDFPJg8LX3UnW17G3wi6rxPJOyCG-52EhLhZkiadg0-9LctxNz63FintuD7MMTcDL6xL7NnRrkIr8b7Wbb8-mV58X12efVtcXF-OdOi4P2MFgaEEFATVXOOzEoX2BgqNChNmSam5KzkQIjRBterQtGyMhig5rQgK0zOsrcH29aFKMdwosRVUVGEBaeJWByIOqiNbDu7Vd2tDMrKu43QNVJ1vdUOJFkxzo2gZYkxVUwpVhLDKoyoQlWhdfL6PJ42rLZQ61Rwim9iOn3j7Vo2YScZQ8mGJ4MPo0EXroeUvtzaqME55SFFt_9uxjAuSZHQd3-hj1c3Uo1KBVhvQjpX703lOa0qXlFSikTNH6HSVcPW6uAhtQ-mgo8TQWJ6uOkbNcQoF79-_gf749_Zq99T9v0Ruwbl-nUc_8M4BekB1F2IsQPz0BCM5H5o7pOT-6GR49Ak2ZvjZj6I7qeE_AEVEBJ4</recordid><startdate>20170713</startdate><enddate>20170713</enddate><creator>Trail, Frances</creator><creator>Wang, Zheng</creator><creator>Stefanko, Kayla</creator><creator>Cubba, Caitlyn</creator><creator>Townsend, Jeffrey P</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>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9890-3907</orcidid></search><sort><creationdate>20170713</creationdate><title>The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi</title><author>Trail, Frances ; Wang, Zheng ; Stefanko, Kayla ; Cubba, Caitlyn ; Townsend, Jeffrey P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-42fe777ed3ad660fbc21ff47ceac45c3f86586e33fcf1db2a489f1eed6423b13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Bayes Theorem</topic><topic>Bayesian analysis</topic><topic>Bioinformatics</topic><topic>Biological Evolution</topic><topic>Biology and Life Sciences</topic><topic>Computer and Information Sciences</topic><topic>Consortia</topic><topic>Developmental biology</topic><topic>Developmental stages</topic><topic>Divergence</topic><topic>Evolution</topic><topic>Evolutionary biology</topic><topic>Fruit bodies</topic><topic>Fruiting Bodies, Fungal - genetics</topic><topic>Funding</topic><topic>Fungi</topic><topic>Fungi - genetics</topic><topic>Gene deletion</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Fungal - genetics</topic><topic>Gene families</topic><topic>Gene Knockout Techniques</topic><topic>Genetic aspects</topic><topic>Genome, Fungal - genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Medicine and Health Sciences</topic><topic>Molds (Fungi)</topic><topic>Morphology</topic><topic>Neurospora crassa - genetics</topic><topic>Observations</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Plant biology</topic><topic>Quality control</topic><topic>Research and Analysis Methods</topic><topic>Roles</topic><topic>Sex Differentiation - genetics</topic><topic>Sordariales - genetics</topic><topic>Sordariales - growth & development</topic><topic>Transcription</topic><topic>Transcription (Genetics)</topic><topic>Transcriptome - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Trail, Frances</creatorcontrib><creatorcontrib>Wang, Zheng</creatorcontrib><creatorcontrib>Stefanko, Kayla</creatorcontrib><creatorcontrib>Cubba, Caitlyn</creatorcontrib><creatorcontrib>Townsend, Jeffrey P</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</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>Trail, Frances</au><au>Wang, Zheng</au><au>Stefanko, Kayla</au><au>Cubba, Caitlyn</au><au>Townsend, Jeffrey P</au><au>Fraser, Hunter B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2017-07-13</date><risdate>2017</risdate><volume>13</volume><issue>7</issue><spage>e1006867</spage><epage>e1006867</epage><pages>e1006867-e1006867</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28704372</pmid><doi>10.1371/journal.pgen.1006867</doi><orcidid>https://orcid.org/0000-0002-9890-3907</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bayes Theorem Bayesian analysis Bioinformatics Biological Evolution Biology and Life Sciences Computer and Information Sciences Consortia Developmental biology Developmental stages Divergence Evolution Evolutionary biology Fruit bodies Fruiting Bodies, Fungal - genetics Funding Fungi Fungi - genetics Gene deletion Gene expression Gene Expression Regulation, Fungal - genetics Gene families Gene Knockout Techniques Genetic aspects Genome, Fungal - genetics Genomes Genomics Medicine and Health Sciences Molds (Fungi) Morphology Neurospora crassa - genetics Observations Phenotype Phenotypes Phylogenetics Phylogeny Plant biology Quality control Research and Analysis Methods Roles Sex Differentiation - genetics Sordariales - genetics Sordariales - growth & development Transcription Transcription (Genetics) Transcriptome - genetics |
title | The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi |
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