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Membrane compartmentalization and signalling

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Group leader : Sébastien Mongrand, Research Director CNRS

Contact :
Phone : 00 33 5 57 12 25 37
email : sebastien.mongrand@u-bordeaux.fr

Sébastien Mongrand is Research Diretcor at the CNRS. He defended his Ph.D. in 1998 at the LBM in chloroplastic lipid biosynthesis. After a three years post-doc at the Rockefeller university (New-York, USA) working on ABA signaling pathway in Nam Hai Chua’s lab, he was recruited CNRS in 2002. He is now leading the “ Domains of the plasma membranes in plants”. He also works in the lipidomic platform as scientific co-leader.

Group members : Mongrand S. (DR), Germain V. (MC), Jolivet M.D. (PhD), Anthony Legrand (PhD), Rocher M. (IE-ANR).

Activity overview :
Plant membranes are highly dynamic cellular compartments. They are made of three main families of lipids : glycerolipids, which often contain highly unsaturated fatty acids, sphingolipids and sterols. They also contain a large amount of proteins (ca 20-30% of protein in the plasma membrane). (Suda et al. 2011). The plasma membrane is continuous between plant cells across intercellular symplastic junctions called plasmodesmata (PD). Permanent re-organisation of membranes sustains the regulation of signalling and exchanges processes and occurs through the formation of specialised membrane domains of different scales (nano or macro domains) which display specific lipids and proteins content. Such sub-compartmentalisation of biological membranes has been described in cyanobacteria, animal and plants (Schaaf et al., 2009 ; Lopez and Kolter, 2010 ; Schmolzer et al, 2011 ; Cacas et al, 2012 ; Li et al, 2012.). The formation of membrane-domains is highly regulated and allows the clustering of specific activities within the membrane (endocytosis, polarisation, signalling, etc). The precise molecular organization of these domains defines physiological activities of membranes and their study is therefore essential for understanding how cells regulate specialised functions at the membrane level. We were pioneers in the characterization of membrane domains at the PM in plants (Mongrand et al, 2004, recent review : Cacas et al, 2012.), which formation is essentially due to sterols and sphingolipids (Roche et al., 2008 ; Morel et al., 2006 ; Lefebvre et al, 2007).
We tackle all these questions on suitable model organisms. Our main objectives are to determine the role of these lipid classes, as well as specific proteins such as Remorin in the structure, fluidity, signal transduction, membrane homeostasis, and dynamics of various membrane functions.

GIPCs, sterols and polyphosphoinositides
Glycosylinositolphosphorylceramides (GIPCs) are the most abundant sphingolipids in plants and fungi (Cacas et al., 2011 Buré et al., 2013, revised Buré et al., 2014). Nevertheless, 50 years after their discovery, GIPCs remain poorly characterized in term of structure and chemical diversity. In addition, their subcellular distributions, their exact structures and biological functions remain poorly understood in plants. To elucidate the structure of these lipids, we developed strategies based on mass spectrometry to analyse their long-chain bases (LCB), Fatty acids (FA) and polar heads (Cacas et al, 2012). We determined that the polar head may contain up to seven monosaccharide sugars (Cacas et al., 2011 Buré et al., 2013, review Buré et al., 2014). Furthermore, GIPCs, sterols and polyphosphoinositides (Furt et al., 2010) are enriched in membrane microdomains of the PM. We recently showed that GIPCs represent up to 60mol% of the lipids in membrane rafts together with free and conjugated sterols (Cacas et al. 2015). GIPCs are the receptor of necrototic toxin of plant pathogen (Lenarcic et al., 2017).

General structure of a typical GIPC.

StREMORIN1.3, a raft-located phosphoprotein, involved in virus propagation and plasmodesmata opening
We have established that StREMORIN1.3 (REM) is a plant raftophilic protein, predominantly associated with sterol- and sphingolipid-rich membrane rafts of approximately 70-nm membrane domains located at the PM and in plasmodesmata (PD) (Raffaele et al., 2009 a and 2009b). This was the first evidence of membrane rafts in plants (for review, Mongrand et al., 2011). We also identified a new C-terminal domain (RemCA) sufficient for anchoring REM to the PM (Perraki et al., 2013). From a manipulation of REM levels in transgenic tomato, we showed that REM is involved in the regulation of viral cell-to-cell movement of Potato virus X (PVX), movement being inversely correlated with REM accumulation (Raffaele et al., 2009).
The novel C-terminal anchor is required for the restriction of Potato Virus X (PVX) movement (Perraki et al., 2013, Gronnier et al. 2017), and affects the ability of the virus to increase PD permeability. By contrast, over-expressed REM does not impair the silencing suppressor activity of the PVX viral protein TGBp1. A similar effect on PD permeability was observed with other movement proteins, suggesting that REM is a general regulator of PD size exclusion limit (Perraki et al., 2014, Gronnier et al. 2017). Finally, we showed that the phosphorylation of REM is necessary for its activation as PD regulator. We showed that the kinase responsible is raft-located. Its activity is stimulated by the presence of the virus. These results add to our knowledge on the mechanisms underlying the role of REM and rafts in virus infection and PD regulation.

REM is anchored to the membrane raft by its C-terminal anchor ; The anchor is essential for REM’s activity toward the restriction of PVX-GFP virus intercellular movement.

Key publications :
- Gronnier J, Crowet JM, Habenstein B, Nasir M, Bayle V, Hosy E, Platre M, Gouguet P, Raffaele S, Martinez D, Grelard A, Loquet A, Simon-Plas F, Gerbeau-Pissot P, Der C, Bayer EM, Jaillais Y, Deleu M, Germain V, Lins L*, Mongrand S* (2017) Structural Basis for Plant Plasma Membrane Protein Dynamics and Organization into Functional Nanodomains. eLife, 6:e26404.
- Lenarčič T, Albert I, Böhm H, Hodnik V, Pirc K, Zavec AB, Podobnik M, Pahovnik D, Žagar E, Pruitt R, Greimel P, Yamaji-Hasegawa A, Kobayashi T, Zienkiewicz A, Gömann J, Mortimer J, Fang L, Mamode-Cassim A, Deleu M, Lins L, Oecking C, Feussner I, Mongrand S, Anderluh G*, Nürnberger T,* (2017) Eudicot plant­specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science, Dec 15 ;358(6369):1431-1434
- Buré C., Cacas JL., Badoc A., Mongrand S. & Schmitter JM. (2016), Branched glycosylated inositolphosphosphingolipid structures in plants revealed by MS3 analysis. Journal of Mass Spectrometry. 51, 305–308.
- Gronnier J, Germain V, Gouguet P, Cacas JL & Mongrand S. (2016). GIPCy king : Glycosyl Inositol Phospho Ceramides, the major sphingolipids on earth. Plant Signaling and Behavior. Review, 11(4):e1152438.
- Cacas JL, Buré C, Grosjean K, Gerbeau-Pissot P, Lherminier J, Rombouts Y, Maes E, Bossard C, Gronnier J, Furt F, Fouillen L, Germain1, Bayer E, Cluzet S, Robert F, Schmitter JM, Deleu M, Lins M, Simon-Plas F, Mongrand S (2015). Re-visiting plant plasma membrane lipids in tobacco : a focus on sphingolipids. Plant Physiology Jan ;170(1):367-84.
- Buré C, Cacas JL, Mongrand S & Schmitter, JM (2014) Characterization of Glycosyl Inositol Phosphoryl Ceramides from Plant and Fungi by Mass Spectrometry (Review). Analytical and Bioanalytical Chemistry, 406(4):995-1010.
- Cacas JL, Buré C, Furt F, Maalouf JP, Badoc A, Cluzet S, Schmitter JM, Antajan E, & Mongrand S (2013) Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity. Phytochemistry, 96:191-200.
- Perraki A, Cacas JL, Crowet JM, Lins L, Castroviejo M, German-Retana S, Mongrand S Raffaele S (2012) Plasma membrane localization of StREM1.3 15 Remorin is mediated by conformational changes in a novel C-terminal anchor and required for the restriction of PVX movement Plant physiology, 160, 1–14.

Collaborators :

F Simon-Plas et P Gerbeau, INRA Dijon
German-Retana S., JP Douliez, BFP INRA Bordeaux
S Raffaele, INRA Toulouse
L Lins et M Deleu, Gembloux Belgique
Y Jaillais, ENS RDP Lyon

Former members :
2002-2003 Damien PALOMO (BTS)
2003-2004 Loïc Cerf (Master 2 RECHERCHE)
2004-2005 David Lafarge (Master 2 RECHERCHE)
2005-2006 Thomas Stanislas (Master 1, Master 2 RECHERCHE
2007-2008 Rémi Zallot (Master 2 RECHERCHE)
2008-2009 Artemis Perraki (Master 2 RECHERCHE, PhD)
2009-2010 Joudia Naj and Fen Wang (Master 2 RECHERCHE)
2011 Maria Binaghi, EMBO short fellowship
2012 Jean-Yves Taburet (BTS)
2012 Zélie Venel (L3)
2012-2016 Julien Gronnier, (Master 2 RECHERCHE, PhD)
2013 Jean-Yves Taburet (BTS)
2013 Clémence Dariceau (L3)
2013 Franco Puccio, (PhD exchange)
2014-2019 Paul Gouguet, (Master 1, Master 2 RECHERCHE, PhD)
2014 Claire Bossard, (Master 2 RECHERCHE)
2016-2020 Adiilah Mamode-Cassim (Master 2 RECHERCHE, PhD)