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An epidermis-driven mechanism positions and scales stem cell niches in plants

Gruel, Jérémy and Landrein, Benoit and Tarr, Paul and Schuster, Christoph and Refahi, Yassin and Sampathkumar, Arun and Hamant, Olivier and Meyerowitz, Elliot M. and Jönsson, Henrik (2016) An epidermis-driven mechanism positions and scales stem cell niches in plants. Science Advances, 2 (1). Art. No. e1500989. ISSN 2375-2548. PMCID PMC4846443. doi:10.1126/sciadv.1500989. https://resolver.caltech.edu/CaltechAUTHORS:20151013-132146207

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Abstract

How molecular patterning scales to organ size is highly debated in developmental biology. We explore this question for the characteristic gene expression domains of the plant stem cell niche residing in the shoot apical meristem. We show that a combination of signals originating from the epidermal cell layer can correctly pattern the key gene expression domains and notably leads to adaptive scaling of these domains to the size of the tissue. Using live imaging, we experimentally confirm this prediction. The identified mechanism is also sufficient to explain de novo stem cell niches in emerging flowers. Our findings suggest that the deformation of the tissue transposes meristem geometry into an instructive scaling and positional input for the apical plant stem cell niche.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1126/sciadv.1500989DOIArticle
http://advances.sciencemag.org/content/2/1/e1500989PublisherArticle
http://advances.sciencemag.org/cgi/content/full/2/1/e1500989/DC1PublisherSupplementary Materials
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4846443/PubMed CentralArticle
ORCID:
AuthorORCID
Landrein, Benoit0000-0002-2371-9996
Schuster, Christoph0000-0002-1948-2367
Sampathkumar, Arun0000-0003-1703-0137
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Additional Information:Copyright © 2016, The Authors. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited. Submitted 24 July 2015. Accepted 30 November 2015. Published 29 January 2016. We thank L. Guignard, G. Malandain, and C. Godin for their help in using MARS for the meristem segmentation. We also thank J. Locke for comments on the manuscript. Funding: This work was funded by grants from the Gatsby Charitable Foundation (GAT3395/PR4) and the Swedish Research Council (VR2013-4632) to H.J. and by Gatsby Charitable Foundation grants GAT3272/C and GAT3273-PR1, the U.S. NIH (R01 GM104244), the Howard Hughes Medical Institute, and the Gordon and Betty Moore Foundation (GBMF3406) (to E.M.M.). Author contributions: J.G. designed the study, performed modeling, collected and analyzed data, and prepared the manuscript. B.L. and P.T. equally contributed in collecting and analyzing data. C.S., Y.R., and A.S. collected and analyzed data. C.S. commented on the manuscript. O.H. and E.M.M. contributed in designing the study and commented on the manuscript. H.J. designed the study and prepared the manuscript. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the corresponding author.
Funders:
Funding AgencyGrant Number
Gatsby Charitable FoundationGAT3395/PR4
Swedish Research CouncilVR2013-4632
Gatsby Charitable FoundationGAT3272/C
Gatsby Charitable FoundationGAT3273-PR1
NIHR01 GM104244
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
Subject Keywords:Stem cells; Shoot apical meristem; Arabidopsis thaliana; WUSCHEL; CLAVATA3; Computational Morphodynamics
Issue or Number:1
PubMed Central ID:PMC4846443
DOI:10.1126/sciadv.1500989
Record Number:CaltechAUTHORS:20151013-132146207
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20151013-132146207
Official Citation:An epidermis-driven mechanism positions and scales stem cell niches in plants BY JÉRÉMY GRUEL, BENOIT LANDREIN, PAUL TARR, CHRISTOPH SCHUSTER, YASSIN REFAHI, ARUN SAMPATHKUMAR, OLIVIER HAMANT, ELLIOT M. MEYEROWITZ, HENRIK JÖNSSON SCIENCE ADVANCES29 JAN 2016 : E1500989
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:61061
Collection:CaltechAUTHORS
Deposited By: Joy Painter
Deposited On:04 Feb 2016 22:15
Last Modified:10 Nov 2021 22:43

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