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Variability in the Control of Cell Division Underlies Sepal Epidermal Patterning in Arabidopsis thaliana

Roeder, Adrienne H. K. and Chickarmane, Vijay and Cunha, Alexandre and Obara, Boguslaw and Manjunath, B. S. and Meyerowitz, Elliot M. (2010) Variability in the Control of Cell Division Underlies Sepal Epidermal Patterning in Arabidopsis thaliana. PLoS Biology, 8 (5). Art. No. e1000367. ISSN 1544-9173. PMCID PMC2867943. doi:10.1371/journal.pbio.1000367. https://resolver.caltech.edu/CaltechAUTHORS:20100709-165015944

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Image (TIFF) (Figure S1. Asynchronous cell cycles and unequal divisions contribute to diversity in cell size.) - Supplemental Material
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Image (TIFF) (Figure S2. lgo mutants block giant cell formation, but not endoreduplication.) - Supplemental Material
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Image (TIFF) (Figure S3. Overexpression of LGO produces ectopic giant cells.) - Supplemental Material
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[img] Video (QuickTime) (Video S1. Live imaging of wild type sepal primordium development. ) - Supplemental Material
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[img] Video (QuickTime) (Video S2. Live imaging of wild type sepal primoridum development.) - Supplemental Material
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[img] Video (QuickTime) (Video S3. Live imaging of wild type sepal primoridum development.) - Supplemental Material
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[img] Video (MPEG) (Video S4. Intercalary Growth model showing early sepal development.) - Supplemental Material
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[img] Video (QuickTime) (Video S5. Live imaging of the formation of the wild sepal primoridum. ) - Supplemental Material
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[img] Video (QuickTime) (Video S6. Live imaging of the apical to basal wave in the termination of cell division in wild sepal development.) - Supplemental Material
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[img] Video (MPEG) (Video S7. Ectopic giant cells computational model. ) - Supplemental Material
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[img] Video (MPEG) (Video S8. Loss of giant cells computational model. ) - Supplemental Material
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[img] Video (QuickTime) (Video S9. Live imaging of pATML1::KRP1 sepal primoridum development. ) - Supplemental Material
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[img] Video (QuickTime) (Video S10. Live imaging of pATML1::KRP1 sepal primoridum development. ) - Supplemental Material
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[img] Video (QuickTime) (Video S11. Live imaging of pATML1::KRP1 sepal primoridum development.) - Supplemental Material
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[img] Video (QuickTime) (Video S12. Live imaging of lgo-1 sepal primoridum development.) - Supplemental Material
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[img] Video (QuickTime) (Video S13. Live imaging of lgo-1 sepal primoridum development. ) - Supplemental Material
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Abstract

How growth and proliferation are precisely controlled in organs during development and how the regulation of cell division contributes to the formation of complex cell type patterns are important questions in developmental biology. Such a pattern of diverse cell sizes is characteristic of the sepals, the outermost floral organs, of the plant Arabidopsis thaliana. To determine how the cell size pattern is formed in the sepal epidermis, we iterate between generating predictions from a computational model and testing these predictions through time-lapse imaging. We show that the cell size diversity is due to the variability in decisions of individual cells about when to divide and when to stop dividing and enter the specialized endoreduplication cell cycle. We further show that altering the activity of cell cycle inhibitors biases the timing and changes the cell size pattern as our model predicts. Models and observations together demonstrate that variability in the time of cell division is a major determinant in the formation of a characteristic pattern.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pbio.1000367DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2867943/PubMed CentralArticle
ORCID:
AuthorORCID
Cunha, Alexandre0000-0002-2541-6024
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2010 Roeder, 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. Received January 11, 2010; Accepted April 1, 2010; Published May 11, 2010. This work was funded by a Helen Hay Whitney Foundation fellowship (http://www.hhwf.org/) (AHKR), the Gordon and Betty Moore Foundation Cell Center (http://www.cellcenter.caltech.edu/) (AHKR and AC), the Department of Energy Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences and Biosciences grant DE-FG02-88ER13873 (EMM), and the National Science Foundation’s ITR#0331697 (BSM), IIS#0808772 (BSM) and FIBR grant EF-0330786 (EMM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Jill Harrison, Carsten Peterson, Marcus Heisler, Eric Mjolsness, and members of the Meyerowitz lab for comments and discussion. We thank Tigran Bacarian for image processing, Rochelle Diamond for expertise on flow cytometry, Aida Sun for technical assistance with mapping, and Cory Tobin for technical assistance with imaging. We thank Keiko Torii for pATML1::KRP1 seeds, Martin Yanofsky for pAS99, Mathew Thompson for pENTR-mC-RCI2A-g, Zachary Nimchuk for creating the monomeric GFP, the Salk Institute Genomic Analysis Laboratory and Arabidopsis Biological Resource Center for lgo-2, and The Arabidopsis Information Resource (TAIR) for essential genome information. Author Contributions: The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: AHKR EMM. Performed the experiments: AHKR. Analyzed the data: AHKR AC BO BSM. Wrote the paper: AHKR VC EMM. Conceived and designed model: AHKR VC EMM. Programmed the computational models: VC. Image processing: AC BO BSM. Academic Editor: Enrico Coen, John Innes Center, United Kingdom.
Funders:
Funding AgencyGrant Number
Helen Hay Whitney FoundationUNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
Department of Energy (DOE)DE-FG02-88ER13873
NSFITR-0331697
NSFIIS-0808772
NSFEF-0330786
Issue or Number:5
PubMed Central ID:PMC2867943
DOI:10.1371/journal.pbio.1000367
Record Number:CaltechAUTHORS:20100709-165015944
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20100709-165015944
Official Citation:Roeder AHK, Chickarmane V, Cunha A, Obara B, Manjunath BS, et al. (2010) Variability in the Control of Cell Division Underlies Sepal Epidermal Patterning in Arabidopsis thaliana. PLoS Biol 8(5): e1000367. doi:10.1371/journal.pbio.1000367
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:18984
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:13 Jul 2010 18:14
Last Modified:08 Nov 2021 23:48

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