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MpFEW RHIZOIDS1 miRNA-mediated lateral inhibition controls rhizoid cell patterning in Marchantia polymorpha

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Thamm, Anna, Saunders, Timothy E. and Dolan, Liam (2020) MpFEW RHIZOIDS1 miRNA-mediated lateral inhibition controls rhizoid cell patterning in Marchantia polymorpha. Current Biology, 30 (10). 1905-1915.e4. doi:10.1016/j.cub.2020.03.032

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Official URL: http://dx.doi.org/10.1016/j.cub.2020.03.032

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Abstract

Lateral inhibition patterns differentiated cell types among equivalent cells during development in bacteria, metazoans, and plants. Tip-growing rhizoid cells develop among flat epidermal cells in the epidermis of the early-diverging land plant Marchantia polymorpha. We show that the majority of rhizoid cells develop individually, but some develop in linear, one-dimensional groups (chains) of between 2 and 7 rhizoid cells in wild-type plants. The distribution of rhizoid cells can be accounted for within a simple cellular automata model of lateral inhibition. The model predicted that in the absence of lateral inhibition, two-dimensional rhizoid cell groups (clusters) form. These can be larger than those formed with lateral inhibition. M. polymorpha rhizoid differentiation is positively regulated by the ROOT HAIR DEFECTIVE SIX-LIKE1 (MpRSL1) basic-helix-loop-helix (bHLH) transcription factor, which is directly repressed by the FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA). To test if MpFRH1 miRNA acts during lateral inhibition, we generated loss-of-function (lof) mutants without the MpFRH1 miRNA. Two-dimensional clusters of rhizoids develop in Mpfrh1lof mutants as predicted by the model for plants that lack lateral inhibition. Furthermore, two-dimensional clusters of up to 9 rhizoid cells developed in the Mpfrh1lof mutants compared to a maximum number of 7 observed in wild-type groups. The higher steady-state levels of MpRSL1 mRNA in Mpfrh1lof mutants indicate that MpFRH1-mediated lateral inhibition involves the repression of MpRSL1 activity. Together, the modeling and genetic data indicate that MpFRH1 miRNA mediates lateral inhibition by repressing MpRSL1 during pattern formation in the M. polymorpha epidermis.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Q Science > QK Botany
Divisions: Faculty of Medicine > Warwick Medical School > Biomedical Sciences
Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): Rhizoids, Cell aggregation, Marchantia -- Spores
Journal or Publication Title: Current Biology
Publisher: Cell Press
ISSN: 0960-9822
Official Date: 18 May 2020
Dates:
DateEvent
18 May 2020Published
2 April 2020Available
12 March 2020Accepted
Volume: 30
Number: 10
Page Range: 1905-1915.e4
DOI: 10.1016/j.cub.2020.03.032
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
PHY-1748958National Science Foundationhttp://dx.doi.org/10.13039/501100008982
R25GM067110National Institutes of Healthhttp://dx.doi.org/10.13039/100000002
2919.01Gordon and Betty Moore Foundationhttp://dx.doi.org/10.13039/100000936
UNSPECIFIEDMechanobiology Institute, Singaporehttp://dx.doi.org/10.13039/501100007672
RGY0083/2016Human Frontier Science Programhttps://www.hfsp.org/
787613 (Denovo-P)European Research Councilhttp://dx.doi.org/10.13039/501100000781
BB/J014427/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
UNSPECIFIEDEdward Penley Abraham Research Fundhttps://register-of-charities.charitycommission.gov.uk/charity-details/?regid=309659&subid=0

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