Combined computational modeling and experimental analysis integrating chemical and mechanical signals suggests possible mechanism of shoot meristem maintenance.
Journal
PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
24
11
2021
accepted:
12
05
2022
revised:
01
07
2022
pubmed:
22
6
2022
medline:
8
7
2022
entrez:
21
6
2022
Statut:
epublish
Résumé
Stem cell maintenance in multilayered shoot apical meristems (SAMs) of plants requires strict regulation of cell growth and division. Exactly how the complex milieu of chemical and mechanical signals interact in the central region of the SAM to regulate cell division plane orientation is not well understood. In this paper, simulations using a newly developed multiscale computational model are combined with experimental studies to suggest and test three hypothesized mechanisms for the regulation of cell division plane orientation and the direction of anisotropic cell expansion in the corpus. Simulations predict that in the Apical corpus, WUSCHEL and cytokinin regulate the direction of anisotropic cell expansion, and cells divide according to tensile stress on the cell wall. In the Basal corpus, model simulations suggest dual roles for WUSCHEL and cytokinin in regulating both the direction of anisotropic cell expansion and cell division plane orientation. Simulation results are followed by a detailed analysis of changes in cell characteristics upon manipulation of WUSCHEL and cytokinin in experiments that support model predictions. Moreover, simulations predict that this layer-specific mechanism maintains both the experimentally observed shape and structure of the SAM as well as the distribution of WUSCHEL in the tissue. This provides an additional link between the roles of WUSCHEL, cytokinin, and mechanical stress in regulating SAM growth and proper stem cell maintenance in the SAM.
Identifiants
pubmed: 35727850
doi: 10.1371/journal.pcbi.1010199
pii: PCOMPBIOL-D-21-02113
pmc: PMC9249181
doi:
Substances chimiques
Arabidopsis Proteins
0
Cytokinins
0
Homeodomain Proteins
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010199Subventions
Organisme : NIGMS NIH HHS
ID : T32 GM136624
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Cell. 2012 Apr 13;149(2):439-51
pubmed: 22500806
J Exp Bot. 2003 Jun;54(387):1585-95
pubmed: 12730267
Development. 2004 Sep;131(17):4225-37
pubmed: 15280208
Nat Rev Mol Cell Biol. 2005 Nov;6(11):850-61
pubmed: 16261190
Elife. 2021 Oct 13;10:
pubmed: 34643181
Curr Opin Plant Biol. 2006 Feb;9(1):83-8
pubmed: 16376602
Planta. 2006 Nov;224(6):1481-4
pubmed: 16775701
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1627-32
pubmed: 16432202
PLoS Genet. 2018 Apr 16;14(4):e1007351
pubmed: 29659567
PLoS Comput Biol. 2007 Apr 27;3(4):e76
pubmed: 17465675
Development. 2019 May 24;146(10):
pubmed: 31076488
Genes Dev. 2011 Oct 1;25(19):2025-30
pubmed: 21979915
PLoS One. 2011 Apr 29;6(4):e18081
pubmed: 21559520
Proc Natl Acad Sci U S A. 2012 Mar 6;109(10):4002-7
pubmed: 22345559
PLoS Comput Biol. 2020 Aug 20;16(8):e1008105
pubmed: 32817654
Trends Plant Sci. 2012 Nov;17(11):666-74
pubmed: 22784824
Plant Signal Behav. 2008 Oct;3(10):853-5
pubmed: 19704520
Philos Trans A Math Phys Eng Sci. 2014 Aug 6;372(2021):
pubmed: 24982253
Proc Natl Acad Sci U S A. 2020 Dec 22;117(51):32731-32738
pubmed: 33288703
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1301-6
pubmed: 16432192
Proc Natl Acad Sci U S A. 2009 May 26;106(21):8453-8
pubmed: 19423667
Phys Biol. 2008 Apr 10;5(1):015002
pubmed: 18403827
Open Biol. 2017 Nov;7(11):
pubmed: 29142108
Plant Physiol. 2001 Jan;125(1):131-4
pubmed: 11154315
Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16529-34
pubmed: 19717465
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1633-8
pubmed: 16415160
Plant Physiol. 2013 Mar;161(3):1066-75
pubmed: 23355633
Annu Rev Cell Dev Biol. 2005;21:203-22
pubmed: 16212493
Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):E4294-303
pubmed: 27436908
Plant J. 1993 Jan;3(1):1-30
pubmed: 8401598
Nature. 2003 Nov 20;426(6964):255-60
pubmed: 14628043
Development. 1996 Jan;122(1):87-96
pubmed: 8565856
Nat Rev Mol Cell Biol. 2001 Jan;2(1):33-9
pubmed: 11413463
Cell Syst. 2019 Jan 23;8(1):53-65.e3
pubmed: 30660611
Curr Opin Plant Biol. 2018 Feb;41:83-88
pubmed: 29073502
Proc Natl Acad Sci U S A. 2011 Apr 12;108(15):6294-9
pubmed: 21383128
Philos Trans R Soc Lond B Biol Sci. 2002 Jun 29;357(1422):737-47
pubmed: 12079669
Phys Biol. 2011 Aug;8(4):045007
pubmed: 21750367
Proc Natl Acad Sci U S A. 2015 Apr 14;112(15):4815-20
pubmed: 25825722
Dev Cell. 2011 Dec 13;21(6):1144-55
pubmed: 22172675
Bull Math Biol. 2019 Aug;81(8):3245-3281
pubmed: 30552627
Am J Bot. 2004 Sep;91(9):1277-93
pubmed: 21652360
Science. 2005 Oct 28;310(5748):663-7
pubmed: 16210497
Science. 2008 Dec 12;322(5908):1650-5
pubmed: 19074340
Phys Biol. 2011 Apr;8(2):026016
pubmed: 21471636
Math Biosci. 2013 May;243(1):1-17
pubmed: 23219575
Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14619-24
pubmed: 25246576
PLoS Comput Biol. 2017 May 22;13(5):e1005533
pubmed: 28531187
Bull Math Biol. 2015 May;77(5):735-8
pubmed: 25980974
Plant Cell. 2008 Apr;20(4):817-9
pubmed: 18441210
New Phytol. 2018 Jul;219(2):505-512
pubmed: 29701870
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):E6298-E6306
pubmed: 27671653
Nat Commun. 2021 Nov 4;12(1):6361
pubmed: 34737298
Dev Biol. 2010 May 1;341(1):95-113
pubmed: 19961843
J R Soc Interface. 2011 Dec 7;8(65):1760-71
pubmed: 21593027
Development. 2003 May;130(10):2027-37
pubmed: 12668618
Proc Natl Acad Sci U S A. 2016 Dec 20;113(51):E8238-E8246
pubmed: 27930326
Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8821-6
pubmed: 15166290
Development. 1998 Apr;125(8):1477-85
pubmed: 9502728
Semin Cell Dev Biol. 2009 Dec;20(9):1126-33
pubmed: 19782146
Curr Opin Plant Biol. 2019 Feb;47:47-55
pubmed: 30261337
Phys Rev E. 2017 Mar;95(3-1):032408
pubmed: 28415180
Development. 2010 Nov;137(21):3581-9
pubmed: 20876644
Plant Cell. 2018 Oct;30(10):2255-2266
pubmed: 30150312