A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control
- Creators
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Refahi, Yassin
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Zardilis, Argyris
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Michelin, Gaël
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Wightman, Raymond
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Leggio, Bruno
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Legrand, Jonathan
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Faure, Emmanuel
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Vachez, Laetitia
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Armezzani, Alessia
- Risson, Anne-Evodie
- Zhao, Feng
- Das, Pradeep
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Prunet, Nathanaël
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Meyerowitz, Elliot M.
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Godin, Christophe
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Malandain, Grégoire
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Jönsson, Henrik
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Traas, Jan
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.
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.Attached Files
Accepted Version - nihms-1740487.pdf
Submitted - 2020.09.25.313312v1.full.pdf
Supplemental Material - 1-s2.0-S1534580721000770-mmc1.pdf
Supplemental Material - 1-s2.0-S1534580721000770-mmc2.xlsx
Supplemental Material - 1-s2.0-S1534580721000770-mmc3.xlsx
Supplemental Material - 1-s2.0-S1534580721000770-mmc4.xlsx
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Additional details
- PMCID
- PMC8519405
- Eprint ID
- 105783
- Resolver ID
- CaltechAUTHORS:20201005-101459275
- European Research Council (ERC)
- 851288
- Agence Nationale pour la Recherche (ANR)
- ANR-19-CE43-0010
- Gene2Shape ERACAPS
- Agence Nationale pour la Recherche (ANR)
- 17-CAPS-0006-01
- Biotechnology and Biological Sciences Research Council (BBSRC)
- BB/S004645/1
- NSF
- IOS-1826567
- Gatsby Charitable Foundation
- GAT3395/PR4B
- Howard Hughes Medical Institute (HHMI)
- Created
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2020-10-05Created from EPrint's datestamp field
- Updated
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2023-07-17Created from EPrint's last_modified field
- Caltech groups
- Division of Biology and Biological Engineering (BBE)