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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 and Godin, Christophe and Malandain, Grégoire and Jönsson, Henrik and Traas, Jan (2020) A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20201005-101459275

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Abstract

The link between gene regulation and morphogenesis of multicellular organisms is a fundamental problem in biology. We address this question in the floral meristem of Arabidopsis, which generates new tissues and organs through complex changes in growth patterns. Starting from high-resolution time-lapse images, we generated a comprehensive 4-D atlas of early flower development including cell lineage, cellular growth rates and the expression patterns of 28 regulatory genes. This information was introduced in MorphoNet, a web-based open-access platform. The application of mechanistic computational models indicated that the molecular network based on the literature only explained a minority of the expression patterns. This was substantially improved by adding single regulatory hypotheses for individual genes. We next used the integrated information to correlate growth with the combinatorial expression of multiple genes. This led us to propose a set of hypotheses for the action of individual genes in morphogenesis, not visible by simply correlating gene expression and growth. This identified the central transcription factor LEAFY as a potential regulator of heterogeneous growth, which was supported by quantifying growth patterns in a leafy mutant. By providing an integrated, multiscale view of flower development, this atlas should represent a fundamental step towards mechanistic multiscale-scale models of flower development.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
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
Meyerowitz, Elliot0000-0003-4798-5153
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. Posted September 26, 2020. The authors would like to thank Arun Sampathkumar, OIivier Hamant and Marie Monniaux for discussion, Anuradha Kar for help with MorphoNet. Weibing Yang provided the lfy mutant and helped with imaging. JT, YR, AA, LV, A-ER and FZ were funded by the ERC grant MORPHOGENETICS. This work was also supported by ANR BIOMOD (ANR-19-CE43-0010) grant (to YR.) and Gene2Shape ERACAPS grant to JT, HJ and AZ. The E.M.M laboratory is funded by the Howard Hughes Medical Institute, and the work here was supported by the U.S. National Science Foundation Division of Integrative Organismal Systems grant IOS1826567. HJ was funded by the Gatsby Charitable Foundation (GAT3395/PR4B) BBSRC (BB/S004645/1). Author contribution: Y.R., A.Z., H.J., 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., G.Ma., contributed new reagents/analytic tools; Y.R., H.J., J.T., A.Z., G.M., J.L, G.Ma., A.A., L.V. and P.D. analyzed data; Y.R.,A.Z., H.J., J.T. wrote the paper. Data Availability: Confocal z-stacks, segmentation files, cell lineage information, and in situ hybridisation images are available online (doi: provided on acceptance). Software scripts for reproducing the analysis performed in this work is available via the Sainsbury Laboratory gitlab repository (https://gitlab.com/slcu/teamhj/publications/refahi_etal_2019). All data is interactively minable via the MorphoNet ATLAS (http://www.morphonet.org).
Funders:
Funding AgencyGrant Number
European Research Council (ERC)MORPHOGENETICS
Agence Nationale pour la Recherche (ANR)ANR-19-CE43-0010
Gene2Shape ERACAPSUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NSFIOS-1826567
Gatsby Charitable FoundationGAT3395/PR4B
Biotechnology and Biological Sciences Research Council (BBSRC)BB/S004645/1
Record Number:CaltechAUTHORS:20201005-101459275
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201005-101459275
Official Citation:A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control. 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 Meyerowitz, Christophe Godin, Grégoire Malandain, Henrik Jönsson, Jan Traas. bioRxiv 2020.09.25.313312; doi: https://doi.org/10.1101/2020.09.25.313312
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:05 Oct 2020 17:48

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