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A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control

Refahi, Yassin and Zardilis, Argyris and Michelin, Gaël and Wightman, Raymond and Leggio, Bruno and Legrand, Jonathan and Faure, Emmanuel and Vachez, Laetitia and Armezzani, Alessia and Risson, Anne-Evodie and Zhao, Feng and Das, Pradeep and Prunet, Nathanaël and Meyerowitz, Elliot M. and Godin, Christophe and Malandain, Grégoire and Jönsson, Henrik and Traas, Jan (2021) A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control. Developmental Cell, 56 (4). pp. 540-556. ISSN 1534-5807. https://resolver.caltech.edu/CaltechAUTHORS:20201005-101459275

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Abstract

We have analyzed the link between the gene regulation and growth during the early stages of flower development in Arabidopsis. Starting from time-lapse images, we generated a 4D atlas of early flower development, including cell lineage, cellular growth rates, and the expression patterns of regulatory genes. This information was introduced in MorphoNet, a web-based platform. Using computational models, we found that the literature-based molecular network only explained a minority of the gene expression patterns. This was substantially improved by adding regulatory hypotheses for individual genes. Correlating growth with the combinatorial expression of multiple regulators led to a set of hypotheses for the action of individual genes in morphogenesis. This identified the central factor LEAFY as a potential regulator of heterogeneous growth, which was supported by quantifying growth patterns in a leafy mutant. By providing an integrated view, this atlas should represent a fundamental step toward mechanistic models of flower development.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.devcel.2021.01.019DOIArticle
https://doi.org/10.1101/2020.09.25.313312DOIDiscussion Paper
https://www.biorxiv.org/content/10.1101/2020.09.25.313312v1OrganizationDiscussion Paper
https://gitlab.com/slcu/teamhj/publications/refahi_etal_2019Related ItemData
http://www.morphonet.orgRelated ItemMorphoNet ATLAS
ORCID:
AuthorORCID
Prunet, Nathanaël0000-0002-8939-5920
Meyerowitz, Elliot M.0000-0003-4798-5153
Godin, Christophe0000-0002-1202-8460
Additional Information:© 2021 Elsevier Inc. Received 17 September 2020, Revised 17 December 2020, Accepted 25 January 2021, Available online 22 February 2021. The authors would like to thank Arun Sampathkumar, OIivier Hamant, and Marie Monniaux for discussion, and Anuradha Kar for help with MorphoNet. Weibing Yang provided the lfy mutant and helped with imaging. J.T., Y.R., A.A., L.V., A.-E.R., and F.Z. were funded by the ERC grant morphogenetics. This work was also supported by ANR BIOMOD (ANR-19-CE43-0010) grant (to Y.R.) and Gene2Shape ERACAPS grant to J.T. (via ANR, 17-CAPS-0006-01), HJ and A.Z. (via BBSRC, BB/S004645/1), E.M.M ( via the U.S. National Science Foundation Division of Integrative Organismal Systems grant IOS1826567, the US part of the Genes2Shape ERACAPS grant). Additional funding was provided by the Gatsby Charitable Foundation to HJ (GAT3395/PR4B). The E.M.M. laboratory is funded by the Howard Hughes Medical Institute. Author contributions: Y.R., A.Z., H.J., and J.T. designed research; Y.R., A.Z., R.W., G.M., J.L., H.J., J.T., A.A., L.V., A.-E.R., P.D., and F.Z. performed research; Y.R., A.Z., H.J., J.T., R.W., G.M., J.L., N.P., F.B., C.G., E.M.M., G. Malandain, B.L., E.F. contributed new reagents/analytic tools; Y.R., H.J., J.T., A.Z., G. Michelin, J.L, G. Malandain, A.A., L.V. and P.D. analyzed data; Y.R., A.Z., H.J., J.T. wrote the paper. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
European Research Council (ERC)851288
Agence Nationale pour la Recherche (ANR)ANR-19-CE43-0010
Gene2Shape ERACAPSUNSPECIFIED
Agence Nationale pour la Recherche (ANR)17-CAPS-0006-01
Biotechnology and Biological Sciences Research Council (BBSRC)BB/S004645/1
NSFIOS-1826567
Gatsby Charitable FoundationGAT3395/PR4B
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:flower development; morphogenesis; molecular network; gene expression
Issue or Number:4
Record Number:CaltechAUTHORS:20201005-101459275
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201005-101459275
Official Citation:Yassin Refahi, Argyris Zardilis, Gaël Michelin, Raymond Wightman, Bruno Leggio, Jonathan Legrand, Emmanuel Faure, Laetitia Vachez, Alessia Armezzani, Anne-Evodie Risson, Feng Zhao, Pradeep Das, Nathanaël Prunet, Elliot M. Meyerowitz, Christophe Godin, Grégoire Malandain, Henrik Jönsson, Jan Traas, A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control, Developmental Cell, Volume 56, Issue 4, 2021, Pages 540-556.e8, ISSN 1534-5807, https://doi.org/10.1016/j.devcel.2021.01.019. (https://www.sciencedirect.com/science/article/pii/S1534580721000770)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105783
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:05 Oct 2020 17:48
Last Modified:23 Feb 2021 17:34

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