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.
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6 March 2023
Article|
February 14 2023
A gene duplication of a septin reveals a developmentally regulated filament length control mechanism
In Special Collection:
Stem Cells and Development 2023
Kevin S. Cannon
,
Kevin S. Cannon
(Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing)
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
2
Department of Biochemistry and Biophysics, University of North Carolina
, Chapel Hill, NC, USA
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Jose M. Vargas-Muniz
,
Jose M. Vargas-Muniz
(Conceptualization, Investigation, Methodology, Visualization, Writing - review & editing)
3
Microbiology Program, School of Biological Sciences, Southern Illinois University
, Carbondale, IL, USA
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Neil Billington
,
Neil Billington
(Investigation)
4
Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health
, Bethesda, MD, USA
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Ian Seim
,
Ian Seim
(Data curation, Formal analysis, Methodology, Software, Visualization, Writing - review & editing)
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
5
Department of Applied Physical Sciences, University of North Carolina
, Chapel Hill, NC, USA
6
Curriculum in Bioinformatics and Computational Biology, University of North Carolina
, Chapel Hill, NC, USA
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Joanne Ekena
,
Joanne Ekena
(Resources)
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
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James R. Sellers
,
James R. Sellers
(Funding acquisition, Resources, Supervision)
4
Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health
, Bethesda, MD, USA
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Amy. S. Gladfelter
(Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing - review & editing)
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
7
Marine Biological Laboratory
, Woods Hole, MA, USA
Correspondence to Amy. S. Gladfelter: amyglad@unc.edu
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Kevin S. Cannon
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
2
Department of Biochemistry and Biophysics, University of North Carolina
, Chapel Hill, NC, USA
Jose M. Vargas-Muniz
Conceptualization, Investigation, Methodology, Visualization, Writing - review & editing
3
Microbiology Program, School of Biological Sciences, Southern Illinois University
, Carbondale, IL, USA
Neil Billington
Investigation
4
Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health
, Bethesda, MD, USA
Ian Seim
Data curation, Formal analysis, Methodology, Software, Visualization, Writing - review & editing
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
5
Department of Applied Physical Sciences, University of North Carolina
, Chapel Hill, NC, USA
6
Curriculum in Bioinformatics and Computational Biology, University of North Carolina
, Chapel Hill, NC, USA
Joanne Ekena
Resources
1
Biology Department, University of North Carolina
, Chapel Hill, NC, USA
James R. Sellers
Funding acquisition, Resources, Supervision
4
Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health
, Bethesda, MD, USA
Correspondence to Amy. S. Gladfelter: amyglad@unc.edu
Disclosures: The authors declare no competing interests exist.
Received:
April 19 2022
Revision Received:
November 20 2022
Accepted:
January 19 2023
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funding
Funder(s):
National Science Foundation
Funder(s):
Division of Molecular and Cellular Biosciences
- Award Id(s): 1615138,2016022
Funder(s):
Howard Hughes Medical Institute
Funder(s):
National Institute of General Medical Sciences
- Award Id(s): T32 GM 119999
Funder(s):
National Institutes of Health
- Award Id(s): 5T32AI052080-14
© 2023 Cannon et al.
2023
Cannon et al.
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/).
J Cell Biol (2023) 222 (3): e202204063.
Article history
Received:
April 19 2022
Revision Received:
November 20 2022
Accepted:
January 19 2023
Connected Content
Citation
Kevin S. Cannon, Jose M. Vargas-Muniz, Neil Billington, Ian Seim, Joanne Ekena, James R. Sellers, Amy. S. Gladfelter; A gene duplication of a septin reveals a developmentally regulated filament length control mechanism. J Cell Biol 6 March 2023; 222 (3): e202204063. doi: https://doi.org/10.1083/jcb.202204063
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