Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast
Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at the species level. Here we generated and analyzed the pan-transcriptome of ~1,000 yeast natural isolates across 4,...
Gespeichert in:
Veröffentlicht in: | Nature genetics 2024-06, Vol.56 (6), p.1278-1287 |
---|---|
Hauptverfasser: | , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 1287 |
---|---|
container_issue | 6 |
container_start_page | 1278 |
container_title | Nature genetics |
container_volume | 56 |
creator | Caudal, Élodie Loegler, Victor Dutreux, Fabien Vakirlis, Nikolaos Teyssonnière, Élie Caradec, Claudia Friedrich, Anne Hou, Jing Schacherer, Joseph |
description | Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at the species level. Here we generated and analyzed the pan-transcriptome of ~1,000 yeast natural isolates across 4,977 core and 1,468 accessory genes. We found that the accessory genome is an underappreciated driver of transcriptome divergence. Global gene expression patterns combined with population structure showed that variation in heritable expression mainly lies within subpopulation-specific signatures, for which accessory genes are overrepresented. Genome-wide association analyses consistently highlighted that accessory genes are associated with proportionally more variants with larger effect sizes, illustrating the critical role of the accessory genome on the transcriptional landscape within and between populations.
Insight from the transcriptomes of 1,032
Saccharomyces cerevisiae
natural isolates emphasizes the essential contribution of accessory genes to the species-level transcriptional landscape. |
doi_str_mv | 10.1038/s41588-024-01769-9 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11176082</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3073676496</sourcerecordid><originalsourceid>FETCH-LOGICAL-c460t-d2dd9d000670a80525f9d1e642eda61fe956e55ffec3e85506896aa71cc663c03</originalsourceid><addsrcrecordid>eNp9kU1v1DAQhiMEoqXlD3BAkbjAwTCOv0-oqlqKtFJ7oGfLdSbbVFl7sZNV99_jNKVAD5xszTzzzsdbVe8ofKbA9JfMqdCaQMMJUCUNMS-qQyq4JFRR_bL8QVLCgcmD6k3OdwCUc9CvqwOmldINZ4cVXrlAxuRC9qnfjnGDdcIduiHXrh5cWmPtvMecY9rXawwz4GMYU38zjX0M9RjnMNZ4v00Fm0M7l3r3kOxDvUeXx-PqVVck8e3je1Rdn5_9OL0gq8tv309PVsRzCSNpm7Y1LQBIBU6DaERnWoqSN9g6STs0QqIQXYeeoRYCpDbSOUW9l5J5YEfV10V3O91ssPVYBnWD3aZ-49LeRtfbfzOhv7XruLOUlgOCborCp0Xh9lndxcnKzjHgwoCmdEcL-_GxW4o_J8yj3fTZ4zC4gHHKloEwjRBGzeiHZ-hdnFIotyiUYlJJbmShmoXyKeacsHuagIKdLbeL5bZYbh8st6YUvf9756eS3x4XgC1ALqmwxvSn939kfwGEtLhu</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3073676496</pqid></control><display><type>article</type><title>Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast</title><source>MEDLINE</source><source>Nature</source><source>Alma/SFX Local Collection</source><creator>Caudal, Élodie ; Loegler, Victor ; Dutreux, Fabien ; Vakirlis, Nikolaos ; Teyssonnière, Élie ; Caradec, Claudia ; Friedrich, Anne ; Hou, Jing ; Schacherer, Joseph</creator><creatorcontrib>Caudal, Élodie ; Loegler, Victor ; Dutreux, Fabien ; Vakirlis, Nikolaos ; Teyssonnière, Élie ; Caradec, Claudia ; Friedrich, Anne ; Hou, Jing ; Schacherer, Joseph</creatorcontrib><description>Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at the species level. Here we generated and analyzed the pan-transcriptome of ~1,000 yeast natural isolates across 4,977 core and 1,468 accessory genes. We found that the accessory genome is an underappreciated driver of transcriptome divergence. Global gene expression patterns combined with population structure showed that variation in heritable expression mainly lies within subpopulation-specific signatures, for which accessory genes are overrepresented. Genome-wide association analyses consistently highlighted that accessory genes are associated with proportionally more variants with larger effect sizes, illustrating the critical role of the accessory genome on the transcriptional landscape within and between populations.
Insight from the transcriptomes of 1,032
Saccharomyces cerevisiae
natural isolates emphasizes the essential contribution of accessory genes to the species-level transcriptional landscape.</description><identifier>ISSN: 1061-4036</identifier><identifier>ISSN: 1546-1718</identifier><identifier>EISSN: 1546-1718</identifier><identifier>DOI: 10.1038/s41588-024-01769-9</identifier><identifier>PMID: 38778243</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/208/199 ; 631/208/200 ; Agriculture ; Animal Genetics and Genomics ; Biochemistry, Molecular Biology ; Biomedical and Life Sciences ; Biomedicine ; Cancer Research ; Cell cycle ; Domestication ; Gene expression ; Gene Expression Profiling - methods ; Gene Expression Regulation, Fungal ; Gene Function ; Genes ; Genetic diversity ; Genetic effects ; Genetic Variation ; Genome, Fungal ; Genome-Wide Association Study ; Genomes ; Genomics ; Genotype ; Genotypes ; Human Genetics ; Life Sciences ; Metabolism ; Microbiology and Parasitology ; Mycology ; Phenotypes ; Phenotypic variations ; Polymorphism, Single Nucleotide ; Population ; Population structure ; Saccharomyces cerevisiae - genetics ; Transcriptome ; Transcriptomes ; Yeast ; Yeasts</subject><ispartof>Nature genetics, 2024-06, Vol.56 (6), p.1278-1287</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>Copyright Nature Publishing Group Jun 2024</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c460t-d2dd9d000670a80525f9d1e642eda61fe956e55ffec3e85506896aa71cc663c03</cites><orcidid>0000-0001-7606-6987 ; 0000-0003-3558-9356 ; 0000-0002-6606-6884 ; 0000-0003-2940-9670</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,782,786,887,27931,27932</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38778243$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04590811$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Caudal, Élodie</creatorcontrib><creatorcontrib>Loegler, Victor</creatorcontrib><creatorcontrib>Dutreux, Fabien</creatorcontrib><creatorcontrib>Vakirlis, Nikolaos</creatorcontrib><creatorcontrib>Teyssonnière, Élie</creatorcontrib><creatorcontrib>Caradec, Claudia</creatorcontrib><creatorcontrib>Friedrich, Anne</creatorcontrib><creatorcontrib>Hou, Jing</creatorcontrib><creatorcontrib>Schacherer, Joseph</creatorcontrib><title>Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast</title><title>Nature genetics</title><addtitle>Nat Genet</addtitle><addtitle>Nat Genet</addtitle><description>Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at the species level. Here we generated and analyzed the pan-transcriptome of ~1,000 yeast natural isolates across 4,977 core and 1,468 accessory genes. We found that the accessory genome is an underappreciated driver of transcriptome divergence. Global gene expression patterns combined with population structure showed that variation in heritable expression mainly lies within subpopulation-specific signatures, for which accessory genes are overrepresented. Genome-wide association analyses consistently highlighted that accessory genes are associated with proportionally more variants with larger effect sizes, illustrating the critical role of the accessory genome on the transcriptional landscape within and between populations.
Insight from the transcriptomes of 1,032
Saccharomyces cerevisiae
natural isolates emphasizes the essential contribution of accessory genes to the species-level transcriptional landscape.</description><subject>631/208/199</subject><subject>631/208/200</subject><subject>Agriculture</subject><subject>Animal Genetics and Genomics</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cancer Research</subject><subject>Cell cycle</subject><subject>Domestication</subject><subject>Gene expression</subject><subject>Gene Expression Profiling - methods</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Gene Function</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genetic effects</subject><subject>Genetic Variation</subject><subject>Genome, Fungal</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype</subject><subject>Genotypes</subject><subject>Human Genetics</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>Microbiology and Parasitology</subject><subject>Mycology</subject><subject>Phenotypes</subject><subject>Phenotypic variations</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Population</subject><subject>Population structure</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><subject>Yeast</subject><subject>Yeasts</subject><issn>1061-4036</issn><issn>1546-1718</issn><issn>1546-1718</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhiMEoqXlD3BAkbjAwTCOv0-oqlqKtFJ7oGfLdSbbVFl7sZNV99_jNKVAD5xszTzzzsdbVe8ofKbA9JfMqdCaQMMJUCUNMS-qQyq4JFRR_bL8QVLCgcmD6k3OdwCUc9CvqwOmldINZ4cVXrlAxuRC9qnfjnGDdcIduiHXrh5cWmPtvMecY9rXawwz4GMYU38zjX0M9RjnMNZ4v00Fm0M7l3r3kOxDvUeXx-PqVVck8e3je1Rdn5_9OL0gq8tv309PVsRzCSNpm7Y1LQBIBU6DaERnWoqSN9g6STs0QqIQXYeeoRYCpDbSOUW9l5J5YEfV10V3O91ssPVYBnWD3aZ-49LeRtfbfzOhv7XruLOUlgOCborCp0Xh9lndxcnKzjHgwoCmdEcL-_GxW4o_J8yj3fTZ4zC4gHHKloEwjRBGzeiHZ-hdnFIotyiUYlJJbmShmoXyKeacsHuagIKdLbeL5bZYbh8st6YUvf9756eS3x4XgC1ALqmwxvSn939kfwGEtLhu</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Caudal, Élodie</creator><creator>Loegler, Victor</creator><creator>Dutreux, Fabien</creator><creator>Vakirlis, Nikolaos</creator><creator>Teyssonnière, Élie</creator><creator>Caradec, Claudia</creator><creator>Friedrich, Anne</creator><creator>Hou, Jing</creator><creator>Schacherer, Joseph</creator><general>Nature Publishing Group US</general><general>Nature Publishing Group</general><scope>C6C</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7606-6987</orcidid><orcidid>https://orcid.org/0000-0003-3558-9356</orcidid><orcidid>https://orcid.org/0000-0002-6606-6884</orcidid><orcidid>https://orcid.org/0000-0003-2940-9670</orcidid></search><sort><creationdate>20240601</creationdate><title>Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast</title><author>Caudal, Élodie ; Loegler, Victor ; Dutreux, Fabien ; Vakirlis, Nikolaos ; Teyssonnière, Élie ; Caradec, Claudia ; Friedrich, Anne ; Hou, Jing ; Schacherer, Joseph</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c460t-d2dd9d000670a80525f9d1e642eda61fe956e55ffec3e85506896aa71cc663c03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>631/208/199</topic><topic>631/208/200</topic><topic>Agriculture</topic><topic>Animal Genetics and Genomics</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cancer Research</topic><topic>Cell cycle</topic><topic>Domestication</topic><topic>Gene expression</topic><topic>Gene Expression Profiling - methods</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Gene Function</topic><topic>Genes</topic><topic>Genetic diversity</topic><topic>Genetic effects</topic><topic>Genetic Variation</topic><topic>Genome, Fungal</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genotype</topic><topic>Genotypes</topic><topic>Human Genetics</topic><topic>Life Sciences</topic><topic>Metabolism</topic><topic>Microbiology and Parasitology</topic><topic>Mycology</topic><topic>Phenotypes</topic><topic>Phenotypic variations</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Population</topic><topic>Population structure</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Transcriptome</topic><topic>Transcriptomes</topic><topic>Yeast</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Caudal, Élodie</creatorcontrib><creatorcontrib>Loegler, Victor</creatorcontrib><creatorcontrib>Dutreux, Fabien</creatorcontrib><creatorcontrib>Vakirlis, Nikolaos</creatorcontrib><creatorcontrib>Teyssonnière, Élie</creatorcontrib><creatorcontrib>Caradec, Claudia</creatorcontrib><creatorcontrib>Friedrich, Anne</creatorcontrib><creatorcontrib>Hou, Jing</creatorcontrib><creatorcontrib>Schacherer, Joseph</creatorcontrib><collection>Springer Nature OA/Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Caudal, Élodie</au><au>Loegler, Victor</au><au>Dutreux, Fabien</au><au>Vakirlis, Nikolaos</au><au>Teyssonnière, Élie</au><au>Caradec, Claudia</au><au>Friedrich, Anne</au><au>Hou, Jing</au><au>Schacherer, Joseph</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast</atitle><jtitle>Nature genetics</jtitle><stitle>Nat Genet</stitle><addtitle>Nat Genet</addtitle><date>2024-06-01</date><risdate>2024</risdate><volume>56</volume><issue>6</issue><spage>1278</spage><epage>1287</epage><pages>1278-1287</pages><issn>1061-4036</issn><issn>1546-1718</issn><eissn>1546-1718</eissn><abstract>Gene expression is an essential step in the translation of genotypes into phenotypes. However, little is known about the transcriptome architecture and the underlying genetic effects at the species level. Here we generated and analyzed the pan-transcriptome of ~1,000 yeast natural isolates across 4,977 core and 1,468 accessory genes. We found that the accessory genome is an underappreciated driver of transcriptome divergence. Global gene expression patterns combined with population structure showed that variation in heritable expression mainly lies within subpopulation-specific signatures, for which accessory genes are overrepresented. Genome-wide association analyses consistently highlighted that accessory genes are associated with proportionally more variants with larger effect sizes, illustrating the critical role of the accessory genome on the transcriptional landscape within and between populations.
Insight from the transcriptomes of 1,032
Saccharomyces cerevisiae
natural isolates emphasizes the essential contribution of accessory genes to the species-level transcriptional landscape.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>38778243</pmid><doi>10.1038/s41588-024-01769-9</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-7606-6987</orcidid><orcidid>https://orcid.org/0000-0003-3558-9356</orcidid><orcidid>https://orcid.org/0000-0002-6606-6884</orcidid><orcidid>https://orcid.org/0000-0003-2940-9670</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1061-4036 |
ispartof | Nature genetics, 2024-06, Vol.56 (6), p.1278-1287 |
issn | 1061-4036 1546-1718 1546-1718 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11176082 |
source | MEDLINE; Nature; Alma/SFX Local Collection |
subjects | 631/208/199 631/208/200 Agriculture Animal Genetics and Genomics Biochemistry, Molecular Biology Biomedical and Life Sciences Biomedicine Cancer Research Cell cycle Domestication Gene expression Gene Expression Profiling - methods Gene Expression Regulation, Fungal Gene Function Genes Genetic diversity Genetic effects Genetic Variation Genome, Fungal Genome-Wide Association Study Genomes Genomics Genotype Genotypes Human Genetics Life Sciences Metabolism Microbiology and Parasitology Mycology Phenotypes Phenotypic variations Polymorphism, Single Nucleotide Population Population structure Saccharomyces cerevisiae - genetics Transcriptome Transcriptomes Yeast Yeasts |
title | Pan-transcriptome reveals a large accessory genome contribution to gene expression variation in yeast |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-07T15%3A51%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Pan-transcriptome%20reveals%20a%20large%20accessory%20genome%20contribution%20to%20gene%20expression%20variation%20in%20yeast&rft.jtitle=Nature%20genetics&rft.au=Caudal,%20%C3%89lodie&rft.date=2024-06-01&rft.volume=56&rft.issue=6&rft.spage=1278&rft.epage=1287&rft.pages=1278-1287&rft.issn=1061-4036&rft.eissn=1546-1718&rft_id=info:doi/10.1038/s41588-024-01769-9&rft_dat=%3Cproquest_pubme%3E3073676496%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3073676496&rft_id=info:pmid/38778243&rfr_iscdi=true |