Cargando…

A gene duplication of a septin reveals a developmentally regulated filament length control mechanism

Septins are a family of conserved filament-forming proteins that function in multiple cellular processes. The number of septin genes within an organism varies, and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear if different combinations of septin proteins i...

Descripción completa

Detalles Bibliográficos
Autores principales: Cannon, Kevin S., Vargas-Muniz, Jose M., Billington, Neil, Seim, Ian, Ekena, Joanne, Sellers, James R., Gladfelter, Amy. S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9960279/
https://www.ncbi.nlm.nih.gov/pubmed/36786832
http://dx.doi.org/10.1083/jcb.202204063
_version_ 1784895475612123136
author Cannon, Kevin S.
Vargas-Muniz, Jose M.
Billington, Neil
Seim, Ian
Ekena, Joanne
Sellers, James R.
Gladfelter, Amy. S.
author_facet Cannon, Kevin S.
Vargas-Muniz, Jose M.
Billington, Neil
Seim, Ian
Ekena, Joanne
Sellers, James R.
Gladfelter, Amy. S.
author_sort Cannon, Kevin S.
collection PubMed
description Septins are a family of conserved filament-forming proteins that function in multiple cellular processes. The number of septin genes within an organism varies, and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear if different combinations of septin proteins in complex alter the polymers’ biophysical properties. We report that a duplication event within the CDC11 locus in Ashbya gossypii gave rise to two similar but distinct Cdc11 proteins: Cdc11a and Cdc1b. CDC11b transcription is developmentally regulated, producing different amounts of Cdc11a- and Cdc11b-complexes in the lifecycle of Ashbya gossypii. Deletion of either gene results in distinct cell polarity defects, suggesting non-overlapping functions. Cdc11a and Cdc11b complexes have differences in filament length and membrane-binding ability. Thus, septin subunit composition has functional consequences on filament properties and cell morphogenesis. Small sequence differences elicit distinct biophysical properties and cell functions of septins, illuminating how gene duplication could be a driving force for septin gene expansions seen throughout the tree of life.
format Online
Article
Text
id pubmed-9960279
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-99602792023-08-14 A gene duplication of a septin reveals a developmentally regulated filament length control mechanism Cannon, Kevin S. Vargas-Muniz, Jose M. Billington, Neil Seim, Ian Ekena, Joanne Sellers, James R. Gladfelter, Amy. S. J Cell Biol Article Septins are a family of conserved filament-forming proteins that function in multiple cellular processes. The number of septin genes within an organism varies, and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear if different combinations of septin proteins in complex alter the polymers’ biophysical properties. We report that a duplication event within the CDC11 locus in Ashbya gossypii gave rise to two similar but distinct Cdc11 proteins: Cdc11a and Cdc1b. CDC11b transcription is developmentally regulated, producing different amounts of Cdc11a- and Cdc11b-complexes in the lifecycle of Ashbya gossypii. Deletion of either gene results in distinct cell polarity defects, suggesting non-overlapping functions. Cdc11a and Cdc11b complexes have differences in filament length and membrane-binding ability. Thus, septin subunit composition has functional consequences on filament properties and cell morphogenesis. Small sequence differences elicit distinct biophysical properties and cell functions of septins, illuminating how gene duplication could be a driving force for septin gene expansions seen throughout the tree of life. Rockefeller University Press 2023-02-14 /pmc/articles/PMC9960279/ /pubmed/36786832 http://dx.doi.org/10.1083/jcb.202204063 Text en © 2023 Cannon et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Cannon, Kevin S.
Vargas-Muniz, Jose M.
Billington, Neil
Seim, Ian
Ekena, Joanne
Sellers, James R.
Gladfelter, Amy. S.
A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title_full A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title_fullStr A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title_full_unstemmed A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title_short A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
title_sort gene duplication of a septin reveals a developmentally regulated filament length control mechanism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9960279/
https://www.ncbi.nlm.nih.gov/pubmed/36786832
http://dx.doi.org/10.1083/jcb.202204063
work_keys_str_mv AT cannonkevins ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT vargasmunizjosem ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT billingtonneil ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT seimian ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT ekenajoanne ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT sellersjamesr ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT gladfelteramys ageneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT cannonkevins geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT vargasmunizjosem geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT billingtonneil geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT seimian geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT ekenajoanne geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT sellersjamesr geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism
AT gladfelteramys geneduplicationofaseptinrevealsadevelopmentallyregulatedfilamentlengthcontrolmechanism