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, in plants, organogenesis and morphogenesis are heavily dependent 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.

Currently, neither the lipid identity at the cell plate nor the molecular mechanisms involved in the guidance and fusion of the cell plate with the plasma membrane are well understood. Whether specific lipids can mark the cortical division zone as well is not known but several lipid mutants defective in phosphoinositides display cytokinesis alterations. Phosphoinositides-mediated cytokinesis probably occurs through the recruitment -and thereby the function- of proteins such as cytoskeleton regulators. Our current knowledge is mainly built on the competencies and tools we have established―and successfully deployed―to further investigate the molecular bases and importance of anionic lipid in cell division orientation.

WE WANT TO ADRESS :

1) How are the anionic lipids and their downstream effectors localized during cell division ?

2) How the lipid homeostatic network controls cell plate fusion at the plasma membrane ?

3) How to build a functional plasma membrane after cytokinesis ?

4) How to build up cell-cell continuity during plant cell division ?

5) What is defining the positioning of the cell division in a plant cell embedded in its tissue ?

Results gained from the ongoing research will provide a better understanding of the signaling mechanisms coupling PIP-metabolism and cell division, the latest being fundamental in regulating organismal growth.

https://twitter.com/Caillaud_MC

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)

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

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.