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
Hauptverfasser: Mamun, Md. Abdulla Al, Katayama, Takuya, Cao, Wei, Nakamura, Shugo, Maruyama, Jun‐ichi
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container_issue 5
container_start_page 964
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creator Mamun, Md. Abdulla Al
Katayama, Takuya
Cao, Wei
Nakamura, Shugo
Maruyama, Jun‐ichi
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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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. 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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. 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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. 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source Wiley-Blackwell Journals; MEDLINE; Wiley Online Library Free Content; EZB Electronic Journals Library
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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