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The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii
Summary Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laborator...
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| Published in: | Molecular microbiology 2017-12, Vol.106 (6), p.949-960 |
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| container_title | Molecular microbiology |
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| creator | Wasserstrom, Lisa Dünkler, Alexander Walther, Andrea Wendland, Jürgen |
| description | Summary
Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laboratory strain is a MATa strain. Here we show that ectopic expression of Saccharomyces cerevisiae MATα2 in A. gossypii completely suppresses sporulation, inhibits riboflavin overproduction and downregulates among others AgSOK2. AgSok2 belongs to a fungal‐specific group of (APSES) transcription factors. Deletion of AgSOK2 strongly reduces riboflavin production and blocks sporulation. The initiator of meiosis, AgIME1, is a transcription factor essential for sporulation. We characterized the AgIME1 promoter region required for complementation of the Agime1 mutant. Reporter assays with AgIME1 promoter fragments fused to lacZ showed that AgSok2 does not control AgIME1 transcription. However, global transcriptome analysis identified two other essential regulators of sporulation, AgIME2 and AgNDT80, as potential targets of AgSok2. Our data suggest that sporulation and riboflavin production in A. gossypii are under mating type locus and nutritional control. Sok2, a target of the cAMP/protein kinase A pathway, serves as a central positive regulator to promote sporulation. This contrasts Saccharomyces cerevisiae where Sok2 is a repressor of IME1 transcription.
Our study has identified a conserved fungal developmental protein of the APSES family as a positive regulator of sporulation in Ashyba gossypii. This regulator, AgSok2, provides an essential link between nutritional signaling via the cAMP‐protein kinase A pathway and the core sporulation machinery including Ime1, Ime2 and Ndt80. Deletion of SOK2 abolishes sporulation; but interestingly, overexpression of the Saccharomyces cerevisiae MATalpha2 repressor also blocks sporulation. Our transcriptomic analyses provide evidence that alpha2 negatively regulates SOK2. |
| doi_str_mv | 10.1111/mmi.13859 |
| format | article |
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Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laboratory strain is a MATa strain. Here we show that ectopic expression of Saccharomyces cerevisiae MATα2 in A. gossypii completely suppresses sporulation, inhibits riboflavin overproduction and downregulates among others AgSOK2. AgSok2 belongs to a fungal‐specific group of (APSES) transcription factors. Deletion of AgSOK2 strongly reduces riboflavin production and blocks sporulation. The initiator of meiosis, AgIME1, is a transcription factor essential for sporulation. We characterized the AgIME1 promoter region required for complementation of the Agime1 mutant. Reporter assays with AgIME1 promoter fragments fused to lacZ showed that AgSok2 does not control AgIME1 transcription. However, global transcriptome analysis identified two other essential regulators of sporulation, AgIME2 and AgNDT80, as potential targets of AgSok2. Our data suggest that sporulation and riboflavin production in A. gossypii are under mating type locus and nutritional control. Sok2, a target of the cAMP/protein kinase A pathway, serves as a central positive regulator to promote sporulation. This contrasts Saccharomyces cerevisiae where Sok2 is a repressor of IME1 transcription.
Our study has identified a conserved fungal developmental protein of the APSES family as a positive regulator of sporulation in Ashyba gossypii. This regulator, AgSok2, provides an essential link between nutritional signaling via the cAMP‐protein kinase A pathway and the core sporulation machinery including Ime1, Ime2 and Ndt80. Deletion of SOK2 abolishes sporulation; but interestingly, overexpression of the Saccharomyces cerevisiae MATalpha2 repressor also blocks sporulation. Our transcriptomic analyses provide evidence that alpha2 negatively regulates SOK2.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.13859</identifier><identifier>PMID: 28985003</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Cyclic AMP-Dependent Protein Kinases - metabolism ; Ectopic expression ; Eremothecium - genetics ; Eremothecium - physiology ; Fragments ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; Gene Deletion ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Fungal ; Kinases ; Mating ; Meiosis ; Promoter Regions, Genetic ; Protein kinase A ; Protein Precursors - genetics ; Protein Precursors - metabolism ; Regulators ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Riboflavin ; Riboflavin - metabolism ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Sporangia ; Spores, Fungal - genetics ; Spores, Fungal - physiology ; Sporulation ; Transcription factors ; Transcription Factors - metabolism ; Vitamin B ; Yeast</subject><ispartof>Molecular microbiology, 2017-12, Vol.106 (6), p.949-960</ispartof><rights>2017 John Wiley & Sons Ltd</rights><rights>2017 John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3889-d43a47d7d4e4944c41d018b8c203513ecbd0a443711a95df34e95be04368039f3</citedby><cites>FETCH-LOGICAL-c3889-d43a47d7d4e4944c41d018b8c203513ecbd0a443711a95df34e95be04368039f3</cites><orcidid>0000-0001-8350-253X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmmi.13859$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.13859$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28985003$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wasserstrom, Lisa</creatorcontrib><creatorcontrib>Dünkler, Alexander</creatorcontrib><creatorcontrib>Walther, Andrea</creatorcontrib><creatorcontrib>Wendland, Jürgen</creatorcontrib><title>The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laboratory strain is a MATa strain. Here we show that ectopic expression of Saccharomyces cerevisiae MATα2 in A. gossypii completely suppresses sporulation, inhibits riboflavin overproduction and downregulates among others AgSOK2. AgSok2 belongs to a fungal‐specific group of (APSES) transcription factors. Deletion of AgSOK2 strongly reduces riboflavin production and blocks sporulation. The initiator of meiosis, AgIME1, is a transcription factor essential for sporulation. We characterized the AgIME1 promoter region required for complementation of the Agime1 mutant. Reporter assays with AgIME1 promoter fragments fused to lacZ showed that AgSok2 does not control AgIME1 transcription. However, global transcriptome analysis identified two other essential regulators of sporulation, AgIME2 and AgNDT80, as potential targets of AgSok2. Our data suggest that sporulation and riboflavin production in A. gossypii are under mating type locus and nutritional control. Sok2, a target of the cAMP/protein kinase A pathway, serves as a central positive regulator to promote sporulation. This contrasts Saccharomyces cerevisiae where Sok2 is a repressor of IME1 transcription.
Our study has identified a conserved fungal developmental protein of the APSES family as a positive regulator of sporulation in Ashyba gossypii. This regulator, AgSok2, provides an essential link between nutritional signaling via the cAMP‐protein kinase A pathway and the core sporulation machinery including Ime1, Ime2 and Ndt80. Deletion of SOK2 abolishes sporulation; but interestingly, overexpression of the Saccharomyces cerevisiae MATalpha2 repressor also blocks sporulation. Our transcriptomic analyses provide evidence that alpha2 negatively regulates SOK2.</description><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>Ectopic expression</subject><subject>Eremothecium - genetics</subject><subject>Eremothecium - physiology</subject><subject>Fragments</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>Gene Deletion</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Kinases</subject><subject>Mating</subject><subject>Meiosis</subject><subject>Promoter Regions, Genetic</subject><subject>Protein kinase A</subject><subject>Protein Precursors - genetics</subject><subject>Protein Precursors - metabolism</subject><subject>Regulators</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Riboflavin</subject><subject>Riboflavin - metabolism</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Sporangia</subject><subject>Spores, Fungal - genetics</subject><subject>Spores, Fungal - physiology</subject><subject>Sporulation</subject><subject>Transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>Vitamin B</subject><subject>Yeast</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNp10F1LwzAUBuAgipsfF_4BCXijF92SnmRNLseYH7DhYBO8K2mbbpntUpNV2b83OvVCMDeHwMPLOS9CF5T0aHj9ujY9CoLLA9SlMOBRLLk4RF0iOYlAxM8ddOL9mhAKZADHqBMLKTgh0EWzxUrj4Ww-nuPG2a02Gzy3LzE2HivcWG-25k1jp5dtpbbWYVti31j3-TN2gwMf-lW2U3hpvd81xpyho1JVXp9_z1P0dDtejO6jyePdw2g4iXIQQkYFA8WSIimYZpKxnNGCUJGJPCbAKeg8K4hiDBJKleRFCUxLnmnCYCAIyBJO0fU-N6z92mq_TWvjc11VaqNt61MqmUg4FwkEevWHrm3rNmG7oBKIkwGVPKibvcpdOMXpMm2cqZXbpZSknzWnoeb0q-ZgL78T26zWxa_86TWA_h68m0rv_k9Kp9OHfeQHMcaEqw</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Wasserstrom, Lisa</creator><creator>Dünkler, Alexander</creator><creator>Walther, Andrea</creator><creator>Wendland, Jürgen</creator><general>Blackwell Publishing Ltd</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8350-253X</orcidid></search><sort><creationdate>201712</creationdate><title>The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii</title><author>Wasserstrom, Lisa ; Dünkler, Alexander ; Walther, Andrea ; Wendland, Jürgen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3889-d43a47d7d4e4944c41d018b8c203513ecbd0a443711a95df34e95be04368039f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Cyclic AMP-Dependent Protein Kinases - metabolism</topic><topic>Ectopic expression</topic><topic>Eremothecium - genetics</topic><topic>Eremothecium - physiology</topic><topic>Fragments</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>Gene Deletion</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Kinases</topic><topic>Mating</topic><topic>Meiosis</topic><topic>Promoter Regions, Genetic</topic><topic>Protein kinase A</topic><topic>Protein Precursors - genetics</topic><topic>Protein Precursors - metabolism</topic><topic>Regulators</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Riboflavin</topic><topic>Riboflavin - metabolism</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Sporangia</topic><topic>Spores, Fungal - genetics</topic><topic>Spores, Fungal - physiology</topic><topic>Sporulation</topic><topic>Transcription factors</topic><topic>Transcription Factors - metabolism</topic><topic>Vitamin B</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wasserstrom, Lisa</creatorcontrib><creatorcontrib>Dünkler, Alexander</creatorcontrib><creatorcontrib>Walther, Andrea</creatorcontrib><creatorcontrib>Wendland, Jürgen</creatorcontrib><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>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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wasserstrom, Lisa</au><au>Dünkler, Alexander</au><au>Walther, Andrea</au><au>Wendland, Jürgen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2017-12</date><risdate>2017</risdate><volume>106</volume><issue>6</issue><spage>949</spage><epage>960</epage><pages>949-960</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Summary
Ashbya gossypii is a homothallic, flavinogenic, filamentous ascomycete that starts overproduction of riboflavin and fragments its mycelium quantitatively into spore producing sporangia at the end of a growth phase. Mating is not required for sporulation and the standard homothallic laboratory strain is a MATa strain. Here we show that ectopic expression of Saccharomyces cerevisiae MATα2 in A. gossypii completely suppresses sporulation, inhibits riboflavin overproduction and downregulates among others AgSOK2. AgSok2 belongs to a fungal‐specific group of (APSES) transcription factors. Deletion of AgSOK2 strongly reduces riboflavin production and blocks sporulation. The initiator of meiosis, AgIME1, is a transcription factor essential for sporulation. We characterized the AgIME1 promoter region required for complementation of the Agime1 mutant. Reporter assays with AgIME1 promoter fragments fused to lacZ showed that AgSok2 does not control AgIME1 transcription. However, global transcriptome analysis identified two other essential regulators of sporulation, AgIME2 and AgNDT80, as potential targets of AgSok2. Our data suggest that sporulation and riboflavin production in A. gossypii are under mating type locus and nutritional control. Sok2, a target of the cAMP/protein kinase A pathway, serves as a central positive regulator to promote sporulation. This contrasts Saccharomyces cerevisiae where Sok2 is a repressor of IME1 transcription.
Our study has identified a conserved fungal developmental protein of the APSES family as a positive regulator of sporulation in Ashyba gossypii. This regulator, AgSok2, provides an essential link between nutritional signaling via the cAMP‐protein kinase A pathway and the core sporulation machinery including Ime1, Ime2 and Ndt80. Deletion of SOK2 abolishes sporulation; but interestingly, overexpression of the Saccharomyces cerevisiae MATalpha2 repressor also blocks sporulation. Our transcriptomic analyses provide evidence that alpha2 negatively regulates SOK2.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28985003</pmid><doi>10.1111/mmi.13859</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-8350-253X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Cyclic AMP-Dependent Protein Kinases - metabolism Ectopic expression Eremothecium - genetics Eremothecium - physiology Fragments Fungal Proteins - genetics Fungal Proteins - metabolism Gene Deletion Gene expression Gene Expression Profiling Gene Expression Regulation, Fungal Kinases Mating Meiosis Promoter Regions, Genetic Protein kinase A Protein Precursors - genetics Protein Precursors - metabolism Regulators Repressor Proteins - genetics Repressor Proteins - metabolism Riboflavin Riboflavin - metabolism Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Sporangia Spores, Fungal - genetics Spores, Fungal - physiology Sporulation Transcription factors Transcription Factors - metabolism Vitamin B Yeast |
| title | The APSES protein Sok2 is a positive regulator of sporulation in Ashbya gossypii |
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