A novel Pezizomycotina‐specific protein with gelsolin domains regulates contractile actin ring assembly and constriction in perforated septum formation
Septum formation in fungi is equivalent to cytokinesis. It differs mechanistically in filamentous ascomycetes (Pezizomycotina) from that of ascomycete yeasts by the retention of a central septal pore in the former group. However, septum formation in both groups is accomplished by contractile actin r...
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Veröffentlicht in: | Molecular microbiology 2020-05, Vol.113 (5), p.964-982 |
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description | Septum formation in fungi is equivalent to cytokinesis. It differs mechanistically in filamentous ascomycetes (Pezizomycotina) from that of ascomycete yeasts by the retention of a central septal pore in the former group. However, septum formation in both groups is accomplished by contractile actin ring (CAR) assembly and constriction. The specific components regulating septal pore organization during septum formation are poorly understood. In this study, a novel Pezizomycotina‐specific actin regulatory protein GlpA containing gelsolin domains was identified using bioinformatics. A glpA deletion mutant exhibited increased distances between septa, abnormal septum morphology and defective regulation of septal pore closure. In glpA deletion mutant hyphae, overaccumulation of actin filament (F‐actin) was observed, and the CAR was abnormal with improper assembly and failure in constriction. In wild‐type cells, GlpA was found at the septum formation site similarly to the CAR. The N‐terminal 329 residues of GlpA are required for its localization to the septum formation site and essential for proper septum formation, while its C‐terminal gelsolin domains are required for the regular CAR dynamics during septum formation. Finally, in this study we elucidated a novel Pezizomycotina‐specific actin modulating component, which participates in septum formation by regulating the CAR dynamics.
Septum formation in multicellular fungi differs by retention of septal pore from that of single cellular yeasts with complete cytokinesis. However, fungal septum formation is commonly regulated by contractile actin ring (CAR) assembly and constriction. This study using comparative genomics identified a novel Pezizomycotina‐specific actin modulating protein GlpA, which regulates septum formation frequency and septal pore closure upon emergency such as cold stress and hyphal wounding. |
doi_str_mv | 10.1111/mmi.14463 |
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Septum formation in multicellular fungi differs by retention of septal pore from that of single cellular yeasts with complete cytokinesis. However, fungal septum formation is commonly regulated by contractile actin ring (CAR) assembly and constriction. This study using comparative genomics identified a novel Pezizomycotina‐specific actin modulating protein GlpA, which regulates septum formation frequency and septal pore closure upon emergency such as cold stress and hyphal wounding.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14463</identifier><identifier>PMID: 31965663</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Actin ; Actin Cytoskeleton - metabolism ; Ascomycota - genetics ; Ascomycota - metabolism ; Aspergillus oryzae ; Aspergillus oryzae - genetics ; Aspergillus oryzae - metabolism ; Assembly ; Bioinformatics ; Cell Division ; Constrictions ; Contractility ; Cytokinesis ; Deletion ; Deletion mutant ; DNA, Fungal - genetics ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; Fungi ; Gelsolin ; Gelsolin - genetics ; Gelsolin - metabolism ; Hyphae ; Kinetics ; Localization ; Morphology ; Mutants ; Mutation ; Pezizomycotina ; Phylogeny ; Protein Domains ; Proteins ; Septum ; Yeasts</subject><ispartof>Molecular microbiology, 2020-05, Vol.113 (5), p.964-982</ispartof><rights>2020 John Wiley & Sons Ltd</rights><rights>2020 John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3883-6fcbdafc0bc808910cf9438fb6352d70f3627a12c5b4bc8dffd06aafcc4fd71a3</citedby><cites>FETCH-LOGICAL-c3883-6fcbdafc0bc808910cf9438fb6352d70f3627a12c5b4bc8dffd06aafcc4fd71a3</cites><orcidid>0000-0002-5318-5366</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.14463$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.14463$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31965663$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mamun, Md. Abdulla Al</creatorcontrib><creatorcontrib>Katayama, Takuya</creatorcontrib><creatorcontrib>Cao, Wei</creatorcontrib><creatorcontrib>Nakamura, Shugo</creatorcontrib><creatorcontrib>Maruyama, Jun‐ichi</creatorcontrib><title>A novel Pezizomycotina‐specific protein with gelsolin domains regulates contractile actin ring assembly and constriction in perforated septum formation</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Septum formation in fungi is equivalent to cytokinesis. It differs mechanistically in filamentous ascomycetes (Pezizomycotina) from that of ascomycete yeasts by the retention of a central septal pore in the former group. However, septum formation in both groups is accomplished by contractile actin ring (CAR) assembly and constriction. The specific components regulating septal pore organization during septum formation are poorly understood. In this study, a novel Pezizomycotina‐specific actin regulatory protein GlpA containing gelsolin domains was identified using bioinformatics. A glpA deletion mutant exhibited increased distances between septa, abnormal septum morphology and defective regulation of septal pore closure. In glpA deletion mutant hyphae, overaccumulation of actin filament (F‐actin) was observed, and the CAR was abnormal with improper assembly and failure in constriction. In wild‐type cells, GlpA was found at the septum formation site similarly to the CAR. The N‐terminal 329 residues of GlpA are required for its localization to the septum formation site and essential for proper septum formation, while its C‐terminal gelsolin domains are required for the regular CAR dynamics during septum formation. Finally, in this study we elucidated a novel Pezizomycotina‐specific actin modulating component, which participates in septum formation by regulating the CAR dynamics.
Septum formation in multicellular fungi differs by retention of septal pore from that of single cellular yeasts with complete cytokinesis. However, fungal septum formation is commonly regulated by contractile actin ring (CAR) assembly and constriction. This study using comparative genomics identified a novel Pezizomycotina‐specific actin modulating protein GlpA, which regulates septum formation frequency and septal pore closure upon emergency such as cold stress and hyphal wounding.</description><subject>Actin</subject><subject>Actin Cytoskeleton - metabolism</subject><subject>Ascomycota - genetics</subject><subject>Ascomycota - metabolism</subject><subject>Aspergillus oryzae</subject><subject>Aspergillus oryzae - genetics</subject><subject>Aspergillus oryzae - metabolism</subject><subject>Assembly</subject><subject>Bioinformatics</subject><subject>Cell Division</subject><subject>Constrictions</subject><subject>Contractility</subject><subject>Cytokinesis</subject><subject>Deletion</subject><subject>Deletion mutant</subject><subject>DNA, Fungal - genetics</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>Fungi</subject><subject>Gelsolin</subject><subject>Gelsolin - genetics</subject><subject>Gelsolin - metabolism</subject><subject>Hyphae</subject><subject>Kinetics</subject><subject>Localization</subject><subject>Morphology</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Pezizomycotina</subject><subject>Phylogeny</subject><subject>Protein Domains</subject><subject>Proteins</subject><subject>Septum</subject><subject>Yeasts</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kb1uFDEQxy0EIkeg4AWQJZpQbGKvvT5vGUUEIiUiBUh0ltcfhyN_LLaX6FLxCLS8Hk-CjwsUSJlmNJrf_DUzfwBeYnSMW5yE4I4xpYw8AitM2ND148AfgxUaB9QR3n8-AM9KuUEIE8TIU3BA8MgGxsgK_DyFMX0zHl6bO3eXwlal6qL89f1HmY1y1ik451SNi_DW1S9wY3xJvlU6BeligdlsFi-rKVClWLNU1XkDdynC7OIGylJMmPwWyqh3TKnZtW6KsBGzyTblNq5hMXNdAmxlkLv2c_DESl_Mi_t8CD6dv_149r67_PDu4uz0slOEc9IxqyYtrUKT4oiPGCk7UsLtxMjQ6zWyhPVriXs1TLQh2lqNmGwDilq9xpIcgqO9brvz62JKFcEVZbyX0aSliJ5QQseR4r6hr_9Db9KSY9tO9BQRTgZOWKPe7CmVUynZWDFnF2TeCozEzi_R_BJ__Grsq3vFZQpG_yP_GtSAkz1w2966fVhJXF1d7CV_AzQrpX0</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Mamun, Md. Abdulla Al</creator><creator>Katayama, Takuya</creator><creator>Cao, Wei</creator><creator>Nakamura, Shugo</creator><creator>Maruyama, Jun‐ichi</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/0000-0002-5318-5366</orcidid></search><sort><creationdate>202005</creationdate><title>A novel Pezizomycotina‐specific protein with gelsolin domains regulates contractile actin ring assembly and constriction in perforated septum formation</title><author>Mamun, Md. Abdulla Al ; Katayama, Takuya ; Cao, Wei ; Nakamura, Shugo ; Maruyama, Jun‐ichi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3883-6fcbdafc0bc808910cf9438fb6352d70f3627a12c5b4bc8dffd06aafcc4fd71a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Actin</topic><topic>Actin Cytoskeleton - metabolism</topic><topic>Ascomycota - genetics</topic><topic>Ascomycota - metabolism</topic><topic>Aspergillus oryzae</topic><topic>Aspergillus oryzae - genetics</topic><topic>Aspergillus oryzae - metabolism</topic><topic>Assembly</topic><topic>Bioinformatics</topic><topic>Cell Division</topic><topic>Constrictions</topic><topic>Contractility</topic><topic>Cytokinesis</topic><topic>Deletion</topic><topic>Deletion mutant</topic><topic>DNA, Fungal - genetics</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>Fungi</topic><topic>Gelsolin</topic><topic>Gelsolin - genetics</topic><topic>Gelsolin - metabolism</topic><topic>Hyphae</topic><topic>Kinetics</topic><topic>Localization</topic><topic>Morphology</topic><topic>Mutants</topic><topic>Mutation</topic><topic>Pezizomycotina</topic><topic>Phylogeny</topic><topic>Protein Domains</topic><topic>Proteins</topic><topic>Septum</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mamun, Md. Abdulla Al</creatorcontrib><creatorcontrib>Katayama, Takuya</creatorcontrib><creatorcontrib>Cao, Wei</creatorcontrib><creatorcontrib>Nakamura, Shugo</creatorcontrib><creatorcontrib>Maruyama, Jun‐ichi</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>Mamun, Md. Abdulla Al</au><au>Katayama, Takuya</au><au>Cao, Wei</au><au>Nakamura, Shugo</au><au>Maruyama, Jun‐ichi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A novel Pezizomycotina‐specific protein with gelsolin domains regulates contractile actin ring assembly and constriction in perforated septum formation</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2020-05</date><risdate>2020</risdate><volume>113</volume><issue>5</issue><spage>964</spage><epage>982</epage><pages>964-982</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Septum formation in fungi is equivalent to cytokinesis. It differs mechanistically in filamentous ascomycetes (Pezizomycotina) from that of ascomycete yeasts by the retention of a central septal pore in the former group. However, septum formation in both groups is accomplished by contractile actin ring (CAR) assembly and constriction. The specific components regulating septal pore organization during septum formation are poorly understood. In this study, a novel Pezizomycotina‐specific actin regulatory protein GlpA containing gelsolin domains was identified using bioinformatics. A glpA deletion mutant exhibited increased distances between septa, abnormal septum morphology and defective regulation of septal pore closure. In glpA deletion mutant hyphae, overaccumulation of actin filament (F‐actin) was observed, and the CAR was abnormal with improper assembly and failure in constriction. In wild‐type cells, GlpA was found at the septum formation site similarly to the CAR. The N‐terminal 329 residues of GlpA are required for its localization to the septum formation site and essential for proper septum formation, while its C‐terminal gelsolin domains are required for the regular CAR dynamics during septum formation. Finally, in this study we elucidated a novel Pezizomycotina‐specific actin modulating component, which participates in septum formation by regulating the CAR dynamics.
Septum formation in multicellular fungi differs by retention of septal pore from that of single cellular yeasts with complete cytokinesis. However, fungal septum formation is commonly regulated by contractile actin ring (CAR) assembly and constriction. This study using comparative genomics identified a novel Pezizomycotina‐specific actin modulating protein GlpA, which regulates septum formation frequency and septal pore closure upon emergency such as cold stress and hyphal wounding.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31965663</pmid><doi>10.1111/mmi.14463</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-5318-5366</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Actin Actin Cytoskeleton - metabolism Ascomycota - genetics Ascomycota - metabolism Aspergillus oryzae Aspergillus oryzae - genetics Aspergillus oryzae - metabolism Assembly Bioinformatics Cell Division Constrictions Contractility Cytokinesis Deletion Deletion mutant DNA, Fungal - genetics Fungal Proteins - genetics Fungal Proteins - metabolism Fungi Gelsolin Gelsolin - genetics Gelsolin - metabolism Hyphae Kinetics Localization Morphology Mutants Mutation Pezizomycotina Phylogeny Protein Domains Proteins Septum Yeasts |
title | A novel Pezizomycotina‐specific protein with gelsolin domains regulates contractile actin ring assembly and constriction in perforated septum formation |
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