Cell wall dynamics stabilize tip growth in a filamentous fungus.
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
08
06
2022
accepted:
22
12
2022
revised:
27
01
2023
pubmed:
18
1
2023
medline:
1
2
2023
entrez:
17
1
2023
Statut:
epublish
Résumé
Hyphal tip growth allows filamentous fungi to colonize space, reproduce, or infect. It features remarkable morphogenetic plasticity including unusually fast elongation rates, tip turning, branching, or bulging. These shape changes are all driven from the expansion of a protective cell wall (CW) secreted from apical pools of exocytic vesicles. How CW secretion, remodeling, and deformation are modulated in concert to support rapid tip growth and morphogenesis while ensuring surface integrity remains poorly understood. We implemented subresolution imaging to map the dynamics of CW thickness and secretory vesicles in Aspergillus nidulans. We found that tip growth is associated with balanced rates of CW secretion and expansion, which limit temporal fluctuations in CW thickness, elongation speed, and vesicle amount, to less than 10% to 20%. Affecting this balance through modulations of growth or trafficking yield to near-immediate changes in CW thickness, mechanics, and shape. We developed a model with mechanical feedback that accounts for steady states of hyphal growth as well as rapid adaptation of CW mechanics and vesicle recruitment to different perturbations. These data provide unprecedented details on how CW dynamics emerges from material secretion and expansion, to stabilize fungal tip growth as well as promote its morphogenetic plasticity.
Identifiants
pubmed: 36649360
doi: 10.1371/journal.pbio.3001981
pii: PBIOLOGY-D-22-01271
pmc: PMC9882835
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3001981Informations de copyright
Copyright: © 2023 Chevalier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
"The authors have declared that no competing interests exist."
Références
Cell Logist. 2012 Jan 1;2(1):2-14
pubmed: 22645705
Curr Biol. 2018 Oct 22;28(20):3342-3351.e3
pubmed: 30318352
Bioessays. 2006 Aug;28(8):799-808
pubmed: 16927300
Dev Cell. 2014 Mar 10;28(5):534-46
pubmed: 24636258
PLoS One. 2011;6(12):e28575
pubmed: 22194856
Nat Rev Microbiol. 2011 Jun 06;9(7):509-18
pubmed: 21643041
J Microsc. 2008 Aug;231(2):265-73
pubmed: 18778424
Eukaryot Cell. 2005 Feb;4(2):225-9
pubmed: 15701784
J Cell Sci. 2022 Nov 1;135(21):
pubmed: 36326245
Cell Microbiol. 2015 Mar;17(3):342-54
pubmed: 25262778
PLoS Comput Biol. 2018 Jan 18;14(1):e1005940
pubmed: 29346368
Mol Biol Cell. 2005 Feb;16(2):918-26
pubmed: 15548594
Curr Opin Microbiol. 2002 Dec;5(6):580-5
pubmed: 12457701
Methods Cell Biol. 2015;125:423-36
pubmed: 25640442
Mycologia. 2008 Nov-Dec;100(6):823-32
pubmed: 19202837
Nat Commun. 2015 Oct 12;6:8400
pubmed: 26455310
iScience. 2022 Jun 02;25(7):104514
pubmed: 35754728
Biophys J. 2011 Oct 19;101(8):1844-53
pubmed: 22004737
Curr Opin Microbiol. 2014 Aug;20:27-33
pubmed: 24858006
Annu Rev Microbiol. 2013;67:587-609
pubmed: 23808332
Biotechnol Prog. 2005 Jan-Feb;21(1):292-9
pubmed: 15903268
PLoS One. 2012;7(10):e46564
pubmed: 23071589
Phys Rev Lett. 2003 Jul 4;91(1):018104
pubmed: 12906580
J Bacteriol. 1986 Dec;168(3):1358-65
pubmed: 3536874
PLoS Biol. 2019 Jan 14;17(1):e2005258
pubmed: 30640903
PLoS Genet. 2018 Apr 02;14(4):e1007291
pubmed: 29608571
Mol Microbiol. 2015 Feb;95(3):491-508
pubmed: 25425159
Biotechnol Adv. 2019 Nov 1;37(6):107352
pubmed: 30797093
Microb Biotechnol. 2009 May;2(3):308-20
pubmed: 21261926
Nat Protoc. 2007;2(4):811-21
pubmed: 17446881
Nat Commun. 2021 Nov 3;12(1):6346
pubmed: 34732740
Microbiology (Reading). 1998 Jan;144 ( Pt 1):45-53
pubmed: 9537763
Mol Biol Cell. 2009 Oct;20(20):4335-47
pubmed: 19692566
Biophys J. 2013 Aug 6;105(3):570-80
pubmed: 23931305
Curr Biol. 2013 Jan 7;23(1):32-41
pubmed: 23200992
Am J Bot. 2012 Sep;99(9):1577-82
pubmed: 22935361
J Theor Biol. 2001 Jan 21;208(2):151-64
pubmed: 11162061
J Cell Sci. 2020 Nov 30;133(22):
pubmed: 33257499
Eukaryot Cell. 2011 Nov;10(11):1504-15
pubmed: 21926329
Sci Adv. 2018 Jan 24;4(1):e1701798
pubmed: 29387789
Eukaryot Cell. 2011 May;10(5):646-53
pubmed: 21335527
Microb Cell. 2019 Jul 15;6(8):335-355
pubmed: 31404395
PLoS One. 2012;7(2):e31218
pubmed: 22359575
Mol Biol Cell. 2019 Apr 1;30(8):975-991
pubmed: 30726171
Methods Cell Biol. 2008;88:3-17
pubmed: 18617025
Mol Biol Cell. 2008 Apr;19(4):1439-49
pubmed: 18216285
Curr Biol. 2015 Aug 17;25(16):2150-7
pubmed: 26212881
Dev Cell. 2018 Apr 23;45(2):170-182.e7
pubmed: 29689193
J Gen Microbiol. 1976 Dec;97(2):169-84
pubmed: 796408
Mol Microbiol. 2007 Dec;66(6):1579-96
pubmed: 18005099
Adv Genet. 2013;81:33-82
pubmed: 23419716
J Bacteriol. 1970 Nov;104(2):989-1009
pubmed: 4099103
J Theor Biol. 2006 Feb 21;238(4):937-48
pubmed: 16105670
J Cell Sci. 2020 May 27;133(10):
pubmed: 32327558
Fungal Genet Biol. 2005 Dec;42(12):963-75
pubmed: 16291501
J Cell Sci. 1981 Apr;48:89-103
pubmed: 7196918
Trends Microbiol. 2022 May;30(5):495-510
pubmed: 35000797
Proc Natl Acad Sci U S A. 2017 May 30;114(22):5701-5706
pubmed: 28507141
Nature. 1989 Apr 20;338(6217):662-4
pubmed: 2649796
Proc Natl Acad Sci U S A. 2019 Jul 9;116(28):13833-13838
pubmed: 31235592
Mol Biol Cell. 2017 Apr 1;28(7):947-961
pubmed: 28209731
Cell Surf. 2018 Apr 13;1:34-42
pubmed: 32743126
Curr Biol. 2007 Feb 20;17(4):347-52
pubmed: 17275302
Curr Opin Microbiol. 2015 Dec;28:36-45
pubmed: 26291501
Mol Biol Cell. 2014 Aug 15;25(16):2428-43
pubmed: 24943841
Microbiol Rev. 1990 Dec;54(4):381-431
pubmed: 2128368
Microsc Microanal. 2016 Apr;22(2):264-74
pubmed: 26879694
Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12228-32
pubmed: 7991610
Dev Cell. 2021 Oct 25;56(20):2856-2870.e7
pubmed: 34666001
Microbiol Spectr. 2017 Apr;5(2):
pubmed: 28429675
Genetics. 2006 Mar;172(3):1557-66
pubmed: 16387870
J Cell Sci. 2008 Dec 1;121(Pt 23):3878-89
pubmed: 18984630
Nat Protoc. 2006;1(6):3111-20
pubmed: 17406574