Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes
Many filamentous ascomycetes develop three-dimensional fruiting bodies for production and dispersal of sexual spores. Fruiting bodies are among the most complex structures differentiated by ascomycetes; however, the molecular mechanisms underlying this process are insufficiently understood. Previous...
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| Veröffentlicht in: | Genetics (Austin) 2019-12, Vol.213 (4), p.1545-1563 |
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| creator | Lütkenhaus, Ramona Traeger, Stefanie Breuer, Jan Carreté, Laia Kuo, Alan Lipzen, Anna Pangilinan, Jasmyn Dilworth, David Sandor, Laura Pöggeler, Stefanie Gabaldón, Toni Barry, Kerrie Grigoriev, Igor V Nowrousian, Minou |
| description | Many filamentous ascomycetes develop three-dimensional fruiting bodies for production and dispersal of sexual spores. Fruiting bodies are among the most complex structures differentiated by ascomycetes; however, the molecular mechanisms underlying this process are insufficiently understood. Previous comparative transcriptomics analyses of fruiting body development in different ascomycetes suggested that there might be a core set of genes that are transcriptionally regulated in a similar manner across species. Conserved patterns of gene expression can be indicative of functional relevance, and therefore such a set of genes might constitute promising candidates for functional analyses. In this study, we have sequenced the genome of the Pezizomycete
, and performed comparative transcriptomics of developing fruiting bodies of this fungus, the Pezizomycete
, and the Sordariomycete
With only 27 Mb, the
genome is the smallest Pezizomycete genome sequenced to date. Comparative transcriptomics indicated that gene expression patterns in developing fruiting bodies of the three species are more similar to each other than to nonsexual hyphae of the same species. An analysis of 83 genes that are upregulated only during fruiting body development in all three species revealed 23 genes encoding proteins with predicted roles in vesicle transport, the endomembrane system, or transport across membranes, and 13 genes encoding proteins with predicted roles in chromatin organization or the regulation of gene expression. Among four genes chosen for functional analysis by deletion in
, three were shown to be involved in fruiting body formation, including two predicted chromatin modifier genes. |
| doi_str_mv | 10.1534/genetics.119.302749 |
| format | Article |
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, and performed comparative transcriptomics of developing fruiting bodies of this fungus, the Pezizomycete
, and the Sordariomycete
With only 27 Mb, the
genome is the smallest Pezizomycete genome sequenced to date. Comparative transcriptomics indicated that gene expression patterns in developing fruiting bodies of the three species are more similar to each other than to nonsexual hyphae of the same species. An analysis of 83 genes that are upregulated only during fruiting body development in all three species revealed 23 genes encoding proteins with predicted roles in vesicle transport, the endomembrane system, or transport across membranes, and 13 genes encoding proteins with predicted roles in chromatin organization or the regulation of gene expression. Among four genes chosen for functional analysis by deletion in
, three were shown to be involved in fruiting body formation, including two predicted chromatin modifier genes.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.119.302749</identifier><identifier>PMID: 31604798</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Ascodesmis nigricans ; Ascomycota ; Ascomycota - genetics ; Asexuality ; BASIC BIOLOGICAL SCIENCES ; Chromatin ; comparative transcriptomics ; Dispersal ; Evolution, Molecular ; Fruit bodies ; Fruiting Bodies, Fungal - genetics ; fruiting body development ; Functional analysis ; Fungi ; Gene deletion ; Gene expression ; Gene Expression Regulation, Fungal ; Genes ; Genes, Mating Type, Fungal ; Genetic Loci ; Genetics ; Genome, Fungal ; Genomes ; Genomics ; Hyphae ; Investigations ; Laboratories ; Membranes ; Molecular modelling ; Phenotype ; Phylogenetics ; Phylogeny ; Proteins ; Puronema confluens ; Secondary Metabolism - genetics ; Sordaria macrospora ; Species ; Spores ; Three dimensional bodies ; Transcription ; Transcriptome - genetics ; Transport</subject><ispartof>Genetics (Austin), 2019-12, Vol.213 (4), p.1545-1563</ispartof><rights>Copyright © 2019 by the Genetics Society of America.</rights><rights>Copyright Genetics Society of America Dec 2019</rights><rights>Copyright © 2019 by the Genetics Society of America 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c460t-7e08b5f5aff0ee318978ecade5e6aef13b664f63da751ea52caea233352cb5be3</citedby><cites>FETCH-LOGICAL-c460t-7e08b5f5aff0ee318978ecade5e6aef13b664f63da751ea52caea233352cb5be3</cites><orcidid>0000-0002-6842-4489 ; 0000-0003-0075-6695 ; 0000-0002-3136-8903 ; 0000000300756695 ; 0000000268424489 ; 0000000231368903</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31604798$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1619142$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Lütkenhaus, Ramona</creatorcontrib><creatorcontrib>Traeger, Stefanie</creatorcontrib><creatorcontrib>Breuer, Jan</creatorcontrib><creatorcontrib>Carreté, Laia</creatorcontrib><creatorcontrib>Kuo, Alan</creatorcontrib><creatorcontrib>Lipzen, Anna</creatorcontrib><creatorcontrib>Pangilinan, Jasmyn</creatorcontrib><creatorcontrib>Dilworth, David</creatorcontrib><creatorcontrib>Sandor, Laura</creatorcontrib><creatorcontrib>Pöggeler, Stefanie</creatorcontrib><creatorcontrib>Gabaldón, Toni</creatorcontrib><creatorcontrib>Barry, Kerrie</creatorcontrib><creatorcontrib>Grigoriev, Igor V</creatorcontrib><creatorcontrib>Nowrousian, Minou</creatorcontrib><creatorcontrib>Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)</creatorcontrib><title>Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Many filamentous ascomycetes develop three-dimensional fruiting bodies for production and dispersal of sexual spores. Fruiting bodies are among the most complex structures differentiated by ascomycetes; however, the molecular mechanisms underlying this process are insufficiently understood. Previous comparative transcriptomics analyses of fruiting body development in different ascomycetes suggested that there might be a core set of genes that are transcriptionally regulated in a similar manner across species. Conserved patterns of gene expression can be indicative of functional relevance, and therefore such a set of genes might constitute promising candidates for functional analyses. In this study, we have sequenced the genome of the Pezizomycete
, and performed comparative transcriptomics of developing fruiting bodies of this fungus, the Pezizomycete
, and the Sordariomycete
With only 27 Mb, the
genome is the smallest Pezizomycete genome sequenced to date. Comparative transcriptomics indicated that gene expression patterns in developing fruiting bodies of the three species are more similar to each other than to nonsexual hyphae of the same species. An analysis of 83 genes that are upregulated only during fruiting body development in all three species revealed 23 genes encoding proteins with predicted roles in vesicle transport, the endomembrane system, or transport across membranes, and 13 genes encoding proteins with predicted roles in chromatin organization or the regulation of gene expression. Among four genes chosen for functional analysis by deletion in
, three were shown to be involved in fruiting body formation, including two predicted chromatin modifier genes.</description><subject>Ascodesmis nigricans</subject><subject>Ascomycota</subject><subject>Ascomycota - genetics</subject><subject>Asexuality</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Chromatin</subject><subject>comparative transcriptomics</subject><subject>Dispersal</subject><subject>Evolution, Molecular</subject><subject>Fruit bodies</subject><subject>Fruiting Bodies, Fungal - genetics</subject><subject>fruiting body development</subject><subject>Functional analysis</subject><subject>Fungi</subject><subject>Gene deletion</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Genes</subject><subject>Genes, Mating Type, Fungal</subject><subject>Genetic Loci</subject><subject>Genetics</subject><subject>Genome, Fungal</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Hyphae</subject><subject>Investigations</subject><subject>Laboratories</subject><subject>Membranes</subject><subject>Molecular modelling</subject><subject>Phenotype</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Puronema confluens</subject><subject>Secondary Metabolism - genetics</subject><subject>Sordaria macrospora</subject><subject>Species</subject><subject>Spores</subject><subject>Three dimensional bodies</subject><subject>Transcription</subject><subject>Transcriptome - genetics</subject><subject>Transport</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkU9v1DAQxSMEoqXwCZCQBZdedus_sRNfkJYtWypV4rKcLceZ7LpK7GA7K20_fb1KWxVOfrJ_82bGryg-E7wknJVXO3CQrIlLQuSSYVqV8k1xTmTJFlQw8vaVPis-xHiPMRaS1--LM0YELitZnxf7tR9GHXSyB0A34PyQHZF2LdoG7aIJdkzz3dajldP98QHQJkw2WbdDP3x7RNdwgN6PA7iErEMb2-uT9lNEq2j8cDSQIH4s3nW6j_Dp6bwo_mx-bte_Fne_b27Xq7uFKQVOiwpw3fCO667DAIzUsqrB6BY4CA0dYY0QZSdYqytOQHNqNGjKGMuq4Q2wi-L77DtOzQCtyZME3asx2EGHo_Laqn9fnN2rnT8oUUvGapENvs4GPiarorEJzN5458AkRQSRpKQZunzqEvzfCWJSg40G-l47yIsryjDHnFN-Qr_9h977KeSfPFGMYkkxLTPFZsoEH2OA7mVigtUpbvUct8pxqznuXPXl9bIvNc_5skeYV6tH</recordid><startdate>20191201</startdate><enddate>20191201</enddate><creator>Lütkenhaus, Ramona</creator><creator>Traeger, Stefanie</creator><creator>Breuer, Jan</creator><creator>Carreté, Laia</creator><creator>Kuo, Alan</creator><creator>Lipzen, Anna</creator><creator>Pangilinan, Jasmyn</creator><creator>Dilworth, David</creator><creator>Sandor, Laura</creator><creator>Pöggeler, Stefanie</creator><creator>Gabaldón, Toni</creator><creator>Barry, Kerrie</creator><creator>Grigoriev, Igor V</creator><creator>Nowrousian, Minou</creator><general>Genetics Society of America</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>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</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>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6842-4489</orcidid><orcidid>https://orcid.org/0000-0003-0075-6695</orcidid><orcidid>https://orcid.org/0000-0002-3136-8903</orcidid><orcidid>https://orcid.org/0000000300756695</orcidid><orcidid>https://orcid.org/0000000268424489</orcidid><orcidid>https://orcid.org/0000000231368903</orcidid></search><sort><creationdate>20191201</creationdate><title>Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes</title><author>Lütkenhaus, Ramona ; Traeger, Stefanie ; Breuer, Jan ; Carreté, Laia ; Kuo, Alan ; Lipzen, Anna ; Pangilinan, Jasmyn ; Dilworth, David ; Sandor, Laura ; Pöggeler, Stefanie ; Gabaldón, Toni ; Barry, Kerrie ; Grigoriev, Igor V ; Nowrousian, Minou</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c460t-7e08b5f5aff0ee318978ecade5e6aef13b664f63da751ea52caea233352cb5be3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Ascodesmis nigricans</topic><topic>Ascomycota</topic><topic>Ascomycota - genetics</topic><topic>Asexuality</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Chromatin</topic><topic>comparative transcriptomics</topic><topic>Dispersal</topic><topic>Evolution, Molecular</topic><topic>Fruit bodies</topic><topic>Fruiting Bodies, Fungal - genetics</topic><topic>fruiting body development</topic><topic>Functional analysis</topic><topic>Fungi</topic><topic>Gene deletion</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Genes</topic><topic>Genes, Mating Type, Fungal</topic><topic>Genetic Loci</topic><topic>Genetics</topic><topic>Genome, Fungal</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Hyphae</topic><topic>Investigations</topic><topic>Laboratories</topic><topic>Membranes</topic><topic>Molecular modelling</topic><topic>Phenotype</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Puronema confluens</topic><topic>Secondary Metabolism - genetics</topic><topic>Sordaria macrospora</topic><topic>Species</topic><topic>Spores</topic><topic>Three dimensional bodies</topic><topic>Transcription</topic><topic>Transcriptome - genetics</topic><topic>Transport</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lütkenhaus, Ramona</creatorcontrib><creatorcontrib>Traeger, Stefanie</creatorcontrib><creatorcontrib>Breuer, Jan</creatorcontrib><creatorcontrib>Carreté, Laia</creatorcontrib><creatorcontrib>Kuo, Alan</creatorcontrib><creatorcontrib>Lipzen, Anna</creatorcontrib><creatorcontrib>Pangilinan, Jasmyn</creatorcontrib><creatorcontrib>Dilworth, David</creatorcontrib><creatorcontrib>Sandor, Laura</creatorcontrib><creatorcontrib>Pöggeler, Stefanie</creatorcontrib><creatorcontrib>Gabaldón, Toni</creatorcontrib><creatorcontrib>Barry, Kerrie</creatorcontrib><creatorcontrib>Grigoriev, Igor V</creatorcontrib><creatorcontrib>Nowrousian, Minou</creatorcontrib><creatorcontrib>Lawrence Berkeley National Lab. 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(LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2019-12-01</date><risdate>2019</risdate><volume>213</volume><issue>4</issue><spage>1545</spage><epage>1563</epage><pages>1545-1563</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><abstract>Many filamentous ascomycetes develop three-dimensional fruiting bodies for production and dispersal of sexual spores. Fruiting bodies are among the most complex structures differentiated by ascomycetes; however, the molecular mechanisms underlying this process are insufficiently understood. Previous comparative transcriptomics analyses of fruiting body development in different ascomycetes suggested that there might be a core set of genes that are transcriptionally regulated in a similar manner across species. Conserved patterns of gene expression can be indicative of functional relevance, and therefore such a set of genes might constitute promising candidates for functional analyses. In this study, we have sequenced the genome of the Pezizomycete
, and performed comparative transcriptomics of developing fruiting bodies of this fungus, the Pezizomycete
, and the Sordariomycete
With only 27 Mb, the
genome is the smallest Pezizomycete genome sequenced to date. Comparative transcriptomics indicated that gene expression patterns in developing fruiting bodies of the three species are more similar to each other than to nonsexual hyphae of the same species. An analysis of 83 genes that are upregulated only during fruiting body development in all three species revealed 23 genes encoding proteins with predicted roles in vesicle transport, the endomembrane system, or transport across membranes, and 13 genes encoding proteins with predicted roles in chromatin organization or the regulation of gene expression. Among four genes chosen for functional analysis by deletion in
, three were shown to be involved in fruiting body formation, including two predicted chromatin modifier genes.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>31604798</pmid><doi>10.1534/genetics.119.302749</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-6842-4489</orcidid><orcidid>https://orcid.org/0000-0003-0075-6695</orcidid><orcidid>https://orcid.org/0000-0002-3136-8903</orcidid><orcidid>https://orcid.org/0000000300756695</orcidid><orcidid>https://orcid.org/0000000268424489</orcidid><orcidid>https://orcid.org/0000000231368903</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1943-2631 |
| ispartof | Genetics (Austin), 2019-12, Vol.213 (4), p.1545-1563 |
| issn | 1943-2631 0016-6731 1943-2631 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6893386 |
| source | MEDLINE; Oxford University Press Journals Current; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Ascodesmis nigricans Ascomycota Ascomycota - genetics Asexuality BASIC BIOLOGICAL SCIENCES Chromatin comparative transcriptomics Dispersal Evolution, Molecular Fruit bodies Fruiting Bodies, Fungal - genetics fruiting body development Functional analysis Fungi Gene deletion Gene expression Gene Expression Regulation, Fungal Genes Genes, Mating Type, Fungal Genetic Loci Genetics Genome, Fungal Genomes Genomics Hyphae Investigations Laboratories Membranes Molecular modelling Phenotype Phylogenetics Phylogeny Proteins Puronema confluens Secondary Metabolism - genetics Sordaria macrospora Species Spores Three dimensional bodies Transcription Transcriptome - genetics Transport |
| title | Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-12T11%3A41%3A45IST&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=Comparative%20Genomics%20and%20Transcriptomics%20To%20Analyze%20Fruiting%20Body%20Development%20in%20Filamentous%20Ascomycetes&rft.jtitle=Genetics%20(Austin)&rft.au=L%C3%BCtkenhaus,%20Ramona&rft.aucorp=Lawrence%20Berkeley%20National%20Lab.%20(LBNL),%20Berkeley,%20CA%20(United%20States)&rft.date=2019-12-01&rft.volume=213&rft.issue=4&rft.spage=1545&rft.epage=1563&rft.pages=1545-1563&rft.issn=1943-2631&rft.eissn=1943-2631&rft_id=info:doi/10.1534/genetics.119.302749&rft_dat=%3Cproquest_pubme%3E2305055252%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=2332092024&rft_id=info:pmid/31604798&rfr_iscdi=true |