Lipid signaling in plant cell division and organogenesis

The coordination of cell division is a crucial process during the development of multicellular organisms. Particularly in organisms where cells are not migrating, like plants, organs, and tissue, patterns are highly correlated to the pattern of cell division. Thus, plant organogenesis and morphogenesis depend heavily on establishing a correct cell division plane. After the separation of the chromosomes, the mother cell will be split in two, giving birth to two daughter cells. The splitting process is called cytokinesis (Fig. 1). In plants, cytokinesis can be broken down into three processes : (i) the establishment of the “cortical division zone” which can be defined as the future site of cell division, (ii) the formation of a membrane-cell wall structure, called the cell plate, that expands towards the plasma membrane of the mother cell through (iii) the insertion of the cell plate to the exact site of division at the plasma membrane to eventually fuse with it. At the end of the cytokinesis, the fully extended cell plate eventually gives rise to the newly formed apicobasal plasma membrane : the correct positioning of this polarity axis through the spatiotemporal coordination of the cell plate fusion is, therefore, a prerequisite to root developmental patterning.

While the importance of division plane orientation for tissue topology and morphogenesis is uncontested, research on division plane positioning primarily focuses on cell-autonomous cues. It has been hypothesized that tissue-scale mechanical stress may influence division plane orientation. Still, how such clues, let alone local tissue topology, are integrated into division plane positioning is unclear.

WE WANT TO ADRESS :

We are currently interested in building an integrating view of the cell division process in a multicellular context and considering the orientation of cell division as a non-cell autonomous mechanism, relying on cues from the local environment.

Using a combined approach of cell biology, molecular genetics, and mechanical modelling at multiscale, we will investigate how plant cells orient their division by integrating biophysical and biochemical signals from surrounding tissues.

In particular, we will address the following questions :

• How does the dividing cell integrate with the local neighbourhood to orient the division plane ?
• What are the molecular cues of the compass incorporating the mechanical and geometrical features to orient cell division ?
• What is the role of maintaining the cell division orientation at the organ scale ?
  Collectively, this work will allow us to build a mechanistic, multi-scale vision of cell division positioning in plants.

WE ARE HIRING !

New opportunities will be soon available with an ERC CoG-funded project, COMPASS starting in October 2025
Stay connected for more details : @mc-caillaud.bsky.social

OUR RESEARCH IS CURRENTLY FUNDED BY :

• FR PROJETS EMERGENTS ENS LYON-2021
• ANR PlantScape (ANR-20-CE13-0026-02)
• ANR DIVCON (ANR-21-CE13-0016-03)
• FR PROJETS EMERGENTS ENS LYON-2023
• ANR/DFG DivFUSE (ANR-22-CE92-0038-02)
• ERC CoG COMPASS (2025-2030)

GROUP MEMBERS :

• CAMILA GOLDI (EMBO Longterm Fellow)
• HORTENSE MOREAU (joint project with Emmanuelle Bayer)
• SAMANTHA MOULIN (Engineer)
• LUCAS COURGEONS (Agregé preparateur)

PAST MEMBERS :

• ELSA GASCON (Engineer, ANR PLANTSCAPE)
• AURELIE FANGAIN (Engineer, ENS)
• ALEXIS LEBECQ (PhD student, ENS)
• MEHDI DOUMANE (PhD Student- 02/2020)
• AMELIE BAUER (Master Student in 2019)

RECENT PUBLICATIONS and PREPRINTS

2024

• Z, P. Li, H, Moreau, J,D. Petit, T, Souza-Moraes, M, Smokvarska, J, Perez-Sancho, M, Petrel, F, Decoeur, L, Brocard, C, Chambaud, M. Grison, A. Paterlini, M. Glavier, L. Hoornaert, A. S. Joshi, E. Gontier, W. A. Prinz, Y. Jaillais, A. Taly, F. Campelo, M-C Caillaud, Emmanuelle M. Bayer* (2024), Plant plasmodesmata bridges form through ER-dependent incomplete cytokinesis. Science 386(6721), 538-545.

2023

• Lebecq. A, C. Goldy, A. Fangain, E. Gascon, K. Belcram, M. Pastuglia, D. Bouchez, M.-C. Caillaud* (2023). The phosphoinositide signature guides the final step of plant cytokinesis. Science Advances

• Goldy C., M. C. Caillaud* (2023) Linking the plant cytoskeleton to membranes via the anionic lipids. Current Opinion in Plant Biology

2022

• Lebecq A., M. Doumane, A. Fangain, V. Bayle, J. Xuan Leong, F. Rozier, M. Marques-Bueno, L. Armengot, R. Boisseau, M. Simon, M. Franz-Wachtel, B. Macek, S. Ustun, Y. Jaillais*, M.-C. Caillaud* (2022) “The Arabidopsis SAC9 Enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the Plasma Membrane” eLife

• Lebecq, A., A. Fangain, A. Boussaroque and M.-C. Caillaud* (2022). "Dynamic Apical-Basal Enrichment of the F-Actin during Cytokinesis in Arabidopsis Cells Embedded in their Tissues." Quantitative Plant Biology

• Caillaud, M. C., (2022) Methods to visualize the Actin Cytoskeleton During Plant Cell Division, (Methods in Molecular Biology), edition Plant Cell Division 10.1007/978-1-0716-1744-1

• Caillaud, M.-C., (2022) Plant cell division : methods and protocols. Preface, (Methods in Molecular Biology), edition Plant Cell Division 10.1007/978-1-0716-1744-1

2021

• Colin, L., R. Martin-Arevalillo, S. Bovio, A. Bauer, T. Vernoux, M. C. Caillaud, B. Landrein and Y. Jaillais (2021). "Imaging the living plant cell : from probes to quantification." https://hal.archives-ouvertes.fr/hal-03359667/document The Plant Cell.

• Saile, S. C., F. M. Ackermann, S. Sunil, J. Keicher, A. Bayless, V. Bonardi, L. Wan, M. Doumane, E. Stöbbe, Y. Jaillais, M.-C. Caillaud, J. L. Dangl, M. T. Nishimura, C. Oecking and F. El Kasmi (2021). "Arabidopsis ADR1 helper NLR immune receptors localize and function at the plasma membrane in a phospholipid dependent manner." New Phytologist 232(6) : 2440-2456.

• Doumane, M., Lebecq, A., Colin, L., Fangain, A., Stevens, F. D., Bareille, J., ... & Caillaud, M. C.* (2021). Inducible depletion of PI(4,5)P2 by the synthetic iDePP system in Arabidopsis. Nature Plants, 7(5), 587-597.

• Noack LC, Bayle V, Armengot L, Roer F, Mamode-Cassim A, Stevens FD, Caillaud MC, Munnik T, Mongrand S, Pleskot R, Jaillais Y. (2021) A nanodomain-anchored scaffolding complex is required for the function and localization of phosphatidylinositol 4-kinase alpha in plants. Plant Cell.
  doi : 10.1093/plcell/koab135

2020 and before

• Doumane, M. and M. C. Caillaud* (2020). "Assessing Extrinsic Membrane Protein Dependency to PI4P Using a Plasma Membrane to Endosome Relocalization Transient Assay in Nicotiana benthamiana." Methods Mol Biol 2177 : 95-108.

• Caillaud, M.-C. (2019) Anionic Lipids : a Pipeline Connecting Key Players of Plant Cell Division. Frontiers in Plant Sciences doi:10.3389/fpls.2019.00419

• Platre, M.P., Noack, L.C., Doumane, M., Bayle, V., Simon, M.L.A., Maneta-Peyret, L., Fouillen, L., Stanislas, T., Armengot, L., Pejchar, P., Caillaud, M.C., Potocky, M., Copic, A., Moreau, P., and Jaillais, Y.2018. A combinatorial lipid code shapes the electrostatic landscape of plant endomembranes. Dev Cell 21 ;45(5):645-480.e11

• Doumane M, Lionnet C, Bayle V, Jaillais Y, Caillaud MC*. Automated Tracking of Root for Confocal Time-lapse Imaging of Cellular Processes. Bio Protoc. 2017 Apr 20 ;7(8). pii : e2245. doi : 10.21769/BioProtoc.2245. PMID : 28459086

• Simon ML, Platre MP, Marquès-Bueno MM, Armengot L, Stanislas T, Bayle V, Caillaud MC*, Jaillais Y*. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nature Plants. 2016 Jun 20 ;2:16089. doi : 10.1038/nplants.2016.89. PMID : 27322096

• Caillaud, M.-C., (2016) Plant cell division : methods and protocols. Preface, (Methods in Molecular Biology, 1370) hal-02799635v1

• Caillaud MC, Wirthmueller L, Sklenar J, Findlay K, Piquerez SJ, Jones AM, Robatzek S, Jones JD, Faulkner C. The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathog. 2014 Nov 13 ;10(10):e1004496.

• Caillaud MC, Paganelli L, Lecomte P, Deslandes L, Quentin M, Pecrix Y, Le Bris M, Marfaing N, Abad P, Favery B. 2009. Spindle assembly checkpoint protein dynamics reveal conserved and unsuspected roles in plant cell division. PLoS One 4 : e6757

• Caillaud, M. C., P. Lecomte, F. Jammes, M. Quentin, S. Pagnotta, E. Andrio, J. de Almeida Engler, N. Marfaing, P. Gounon, P. Abad and B. Favery (2008). "MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis." Plant Cell 20(2) : 423-437.