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SMS

SYMBIOTIC SIGNALING

Our group analyzes the molecular mechanisms that allow recognition between plants and microorganisms leading to the establishment of beneficial symbiotic interactions of great agronomic importance.
 
We are more particularly interested on the one hand in the nitrogen fixing symbiosis between plants of the legume family and rhizobia bacteria (LR symbiosis), which allows legumes to grow without the addition of nitrogen fertilizers, and on the other part in the symbiosis that associates most higher plants and the arbuscular mycorrhizal fungi (AM symbiosis), which facilitates the absorption of nutrients and water present in the soil. The establishment of these two evolutionarily related symbioses involves microbial signals of similar structures, which activate the same signaling pathway in the plant, called the Common Symbiotic Signaling Pathway (CSSP).
 
Using genetic, biochemical, genomic and cellular approaches, we study microbial signals as well as receptors / components of the signal transduction pathway which, in plants, activate CSSP. Our work is based on the study of model plants (the legume Medicago truncatula and the monocotyledonous plant Brachypodium distachyon), but also concerns the transposition of our results to field plants such as peas, soybeans or wheat.
 
By understanding the mechanisms of symbiotic signaling, our work aims to improve the use of symbiotic signals and beneficial symbioses for sustainable agriculture.

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RESEARCH THEMES

Signaling Nod factors

For LR symbiosis, we have shown that CSP is activated by secreted bacterial lipochito-oligosaccharide (LCO) signals, called Nod factors. These signals are necessary for infection and organogenesis of the nodule, and are perceived by lysine-patterned receptor kinases (LysM-RLKs). One of the group's main projects focuses on the regulation and function of LysM-RLK proteins in M.truncatula, through a combination of molecular, biochemical, genetic and cell biology approaches.

 

The ability of proteins and receptor complexes to bind to Nod factors is also studied. In addition, we seek to analyze how activation of LysM-RLKs allows signal transduction to downstream elements. This work involves the study of different proteins involved in signal transduction as well as of symbiotic receptor interactors. In this way, we aim to understand how the host legume perceives the specific Nod factors of the rhizobial symbiont, and how these signals are transduced to activate the plant's symbiotic responses.

Mycorrhizal symbiotic signaling

Regarding the AM symbiosis, a recent collaboration with Guillaume Bécard (UMR CNRS / UPS 5546) and Vérena Poinsot (UMR CNRS / UPS 5623) allowed us to show that the mycorrhizal fungus Rhizophagus irregularis produces sulphated and non-sulphated lipochitooligosaccharide signals , called Myc-LCOs.

 

These signals activate CSP, lead to induction of gene expression and root system branching in M. truncatula, and stimulate AM formation in various plant families. Using Myc-LCOs synthesized by H. Driguez and colleagues at CERMAV, Grenoble, we continue to dissect the mechanisms by which host plants perceive mycorrhizal fungi and activate downstream responses.

Developmental effects and agronomic use of symbiotic signals

Since Nod and Myc factors are able to stimulate secondary root formation in M. truncatula, we are studying the signaling mechanisms controlling this response by combining cell biology and transcriptomic approaches with the use of mutants of M. truncatula affected for induction of these secondary roots by Nod / Myc factors.

 

The ability of Nod factors to act as growth regulators has led to the commercialization by Novozymes (formerly EMD Crop BioScience) of rhizobium inoculants enriched with Nod factors for soybeans, peanuts, alfalfa and peas. This work is now continuing to determine whether Myc LCOs compounds also have growth regulating activity on a broad spectrum of plants, and whether processing of seeds with these signals stimulates root development and / or mycorrhization.

Genomics of Medicago truncatula

Our work on the dissection of the mechanisms of perception / transduction of the symbiotic signal has made extensive use of genetic and genomic tools developed by the international scientific community for M. truncatula. We have contributed to the International Genome Sequencing Project of M. truncatula by sequencing chromosome 5, in collaboration with the Génoscope (Evry) ( http://medicago.org/genome ).

Collaborations

Our collaborators for Nod factor signaling are the groups of David Barker and Pascal Gamas (LIPM), René Geurts and Ton Bisseling (Wageningen Univeristy, The Netherlands), Theodorus Gadella (Amsterdam University, The Netherlands), Jean-Michel Ané (Wisconsin University ), L. Gentzbittel (SP2, ENSAT), and Thomas Ott (University of Munich).

Our collaborators for mycorrhizal symbiotic signaling are the groups of Guillaume Bécard (UMR CNRS / UPS 5546) and Vérena Poinsot (UMR CNRS / UPS 5623).

Our collaborators for the LCO synthesis are the groups of Jean-Marie Beau (Orsay, Paris) and Sébastien Fort (CERMAV, Grenoble).

Our collaborators for genomic studies are J. Gouzy (LIPM), Francis Quétier and collaborators (Génoscope-CEA Paris), and The International consortium for the genome sequencing project for Medicago truncatula: Nevin Young (University of Minnesota, USA), Chris Town (JCVI, USA), Bruce Roe (University of Oklahoma, USA), René Geurts (Wageningen University, The Netherlands), Giles Oldroyd andJane Rogers (JIC, UK).

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MEMBERS

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  • Du D, Zhang C, Xing Y, Lu X, Cai L, Yun H, Zhang Q, Zhang Y, Chen X, Liu M, Sang X, Ling Y, Yang Z, Li Y, Lefebvre B, He G (2020) The CC-NB-LRR OsRLR1 mediates rice disease resistance through interaction with OsWRKY19. Plant Biotechnol J, in press
     

     

  • Maillet F, Fournier J, Mendis HC, Tadege M, Wen J, Ratet P, Mysore KS, Gough C, Jones KM. 2020. Sinorhizobium meliloti succinylated high-molecular-weight succinoglycan and the Medicago truncatula LysM receptor-like kinase MtLYK10 participate independently in symbiotic infection. Plant J. 102: 311-326
     

     

  • Lefebvre B. 2020. An opportunity to breed rice for improved benefits from the arbuscular mycorrhizal symbiosis? New Phytol, 225: 1404-1406 
     

     

  • Carrère S, Verdenaud M, Gough C, Gouzy J, Gamas P. 2019. LeGOO: An Expertized Knowledge Database for the Model Legume Medicago truncatula. Plant Cell Physiol, 16: 203-2011
     

     

  • Girardin A, Wang T, Ding Y, Keller J, Buendia L, Gaston M, Ribeyre C, Gasciolli V, Auriac MC, Vernié T, Bendahmane A, Ried MK, Parniske M, Vandenbussche M, Schorderet M, Reinhardt D, Delaux PM, Bono JJ and Lefebvre B. 2019. LCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biol, 29: 4249-4259
     

     

  • Buendia L, Ribeyre C, Bensmihen S, Lefebvre B. 2019. Brachypodium distachyon tar2lhypo mutant shows reduced root developmental response to symbiotic signal but increased arbuscular mycorrhiza. Plant Signal Behav 14: e1651608.
     

     

  • Sorroche F, Walch M, Zou L, Rengel D, Maillet F, Gibelin-Viala C, Poinsot V, Chervin C, Masson-Boivin C, Gough C, Batut J, Garnerone AM. 2019. Endosymbiotic Sinorhizobium meliloti modulate Medicago root susceptibility to secondary infection via ethylene. New Phytol, 223:1505-1515.
     

     

  • Gibelin-Viala C, Amblard E, Puech-Pages V, Bonhomme M, Garcia M, Bascaules-Bedin A, Fliegmann J, Wen J, Mysore KS, le Signor C, Jacquet C, Gough C. 2019. The Medicago truncatula LysM receptor-like kinase LYK9 plays a dual role in immunity and the arbuscular mycorrhizal symbiosis. New Phytol, 223:1516-1529.
     

     

  • Rey T, André O, Nars A, Dumas B, Gough C, Bottin A, Jacquet C. 2019. Lipo-chitooligosaccharide signalling blocks a rapid pathogen-induced ROS burst without impeding immunity. New Phytol. 221: 743-749
     

     

  • Buendia L., Maillet F., O’Connor D., van de-Kerkhove Q., Danoun S., Gough C., Lefebvre B. and Bensmihen S. 2019. LCOs promote lateral root formation and modify auxin homeostasis in Brachypodium distachyon. New Phytol, 221: 2190-2202
     

     

  • Buendia L., Girardin A., Wang T., Cottret L. and Lefebvre B. 2018 LysM Receptor-Like Kinase and LysM Receptor-Like Protein Families: An Update on Phylogeny and Functional Characterization. Front. Plant Sci. 9:1531
     

     

  • Buhian W.P. and Bensmihen S. 2018. Nod Factor Regulation of Phytohormone Signaling and Homeostasis During Rhizobia-Legume Symbiosis. Front. Plant Sci. 9:1247
     

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    Herrbach V., Maillet F. and Bensmihen S. 2018. Adapting the Lateral Root-Inducible System to Medicago truncatula. Methods Mol Biol. 1761:77-83
     

     

  • Sevin-Pujol A., Sicard M., Rosenberg C., Auriac M.C., Lepage A., Niebel A., Gough C. and Bensmihen S. 2018. Development of a GAL4-VP16/UAS trans-activation system for tissue specific expression in Medicago truncatula. PLoS One. 12:e0188923
     

     

  • Gough C., Cottret L., Lefebvre B. and Bono JJ. 2018. Evolutionary History of Plant LysM Receptor Proteins Related to Root Endosymbiosis. Front Plant Sci. 9:923
     

     

  • Lefebvre B. 2017. Arbuscular mycorrhiza: A new role for N-acetylglucosamine. Nature Plants 3, 17085
     

     

  • Herrbach V., Chirinos X., Rengel D., Agbevenou K., Vincent R., Pateyron S., Huguet S., Balzergue S., Pasha A., Provart N., Gough C. and Bensmihen S. 2017. Nod factors potentiate auxin signaling for transcriptional regulation and lateral root formation in Medicago truncatula. J Exp Bot. 68:569-583
     

     

  • Fliegmann J., Jauneau A., Pichereaux C., Rosenberg C., Gasciolli V., Timmers A.C., Burlet-Schiltz O., Cullimore J. and Bono J.J. 2016. LYR3, a high-affinity LCO-binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor. FEBS Lett 590:1477-87
     

     

  •  Malkov N., Fliegmann J., Rosenberg C., Gasciolli V., Timmers A.C., Nurisso A., Cullimore J., Bono J.J. 2016. Molecular basis of lipo-chitooligosaccharide recognition by the lysin motif receptor-like kinase LYR3 in legumes. Biochem J 473:1369-78
     

     

  • Vernié T., Camut S., Camps C., Rembliere C., de Carvalho-Niebel F., Mbengue M., Timmers T., Gasciolli V., Thompson R., Le Signor C., Lefebvre B., Cullimore J. and Hervé C. 2016. PUB1 interacts with the receptor kinase DMI2 and negatively regulates rhizobial and arbuscular mycorrhizal symbioses through its ubiquitination activity in Medicago truncatula. Plant Physiol, 170: 2312-2324. 
     

     

  • Buendia L., Wang T., Girardin A.  and Lefebvre B. 2016. The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato. New Phytol 210, 184-195. 
     

     

  • Camps C., Jardinaud M.F., Rengel D., Carrère S., Hervé C., Debellé F., Gamas P., Bensmihen S. and Gough C. 2015. Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc-LCOs in Medicago truncatula. New Phytol 208: 224-240. 
     

     

  • Gonzalez A. A., Agbévénou K., Herrbach V., Gough C., Bensmihen S. Abscisic acid promotes pre-emergence stages of lateral root development in Medicago truncatula. 2015.Plant Signal Behav 10(1):e977741. 
     

     

  • Gough C, Jacquet C. 2013. Nod factor perception protein carries weight in biotic interactions. Trends Plant Sci. 10: 566-74.
     

     

  • Herrbach V, Remblière C, Gough C, Bensmihen S. 2013. Lateral root formation and patterning in Medicago truncatula. J Plant Physiol pii: S0176-1617(13)00362-3. 
     

     

  • Fliegmann J., Canova S., Lachaud C., Uhlenbroich S., Gasciolli V., Pichereaux C., Rossignol M., Rosenberg C., Cumener M., Pitorre D., Lefebvre B., Gough C., Samain E., Fort S., Driguez H., Vauzeilles B., Beau J.M., Nurisso A., Imberty A., Cullimore J. and Bono J.J. 2013. Lipo-chitooligosaccharidic symbiotic signals are recognized by the LysM receptor like kinase LYR3 in the legume Medicago truncatula. ACS Chemical Biology 8: 1900-1906. 
     

     

  • Pietraszewska-Bogiel A., Lefebvre B., Koini M.A., Klaus-Heisen D., Takken F.L.W., Geurts R., Cullimore J.V and Gadella T.W.J. 2013. Interaction of Medicago truncatula Lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamianaleaf induces a defence-like response. PlosOne 8(6):e65055 
     

     

  • Park C.J., Sharma R., Lefebvre B., Canlas P.E, and Ronald P.C. 2013. Endoplasmic reticulum-quality control component SDF2 is essential for XA21-mediated immunity in rice. Plant Science 210:53-60 
     

     

  • Rival P, Bono JJ, Gough C, Bensmihen S, Rosenberg C. 2013. Cell autonomous and non-cell autonomous control of rhizobial and mycorrhizal infection in Medicago truncatula. Plant Signal Behav 6;8(2). 
     

     

  • Rival P, de Billy F, Bono JJ, Gough C, Rosenberg C, Bensmihen S. 2012. Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development ; 139:3383-91. 
     

     

  • Lefebvre B, Klaus-Heisen D, Pietraszewska-Bogiel A, Hervé C, Camut S, Auriac MC, Gasciolli V, Nurisso A, Gadella TW, Cullimore J. 2012. Role of N-glycosylation sites and CxC motifs in trafficking of Medicago truncatula Nod Factor Perception protein to plasma membrane. J Biol Chem 287: 10812-10823. 
     

     

  • Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, Mysore KS, Dénarié J, Schultze M, Oldroyd GE. 2012. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol. 22(23):2236-41.
     

     

  • Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, Samain E, Dénarié J, Küster H, Hohnjec N. 2012. Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol. 159(4):1671-85. 
     

     

  • Bensmihen S, De Billy, F, Gough C. 2011. Contribution of NFP LysM domains to the recognition of Nod Factors during the Medicago truncatula/ Sinorhizobium meliloti symbiotic interaction. PLoS ONE  6(11): 11. 
     

     

  • Debellé F, Young ND, Oldroyd GE et al. 2011.  The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature. 16;480(7378):520-4 
     

     

  • Gough, C. and Cullimore, J. 2011. Lipo-chitooligosaccharide signalling in endosymbiotic plant-microbe interactions. Mol. Plant-Microbe Interact. 24(8):867-878. 
     

     

  • Herve, C., Lefebvre, B., Cullimore, J. 2011. How many E3 ubiquitin ligases are involved in the regulation of nodulation? Plant Signal. Behav 6(5):660-664. 
     

     

  • Fliegmann, J., Uhlenbroich, S., Shinya, T., Martinez, Y., Lefebvre, B., Shibuya, N., Bono, J.J. 2011. Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Phys. Biochem. 49(7):709-720. 
     

     

  • Klaus-Heisen, D., Nurisso, A., Pietraszewska-Bogiel, A., Mbengue, M., Camut, S., Timmers, T., Pichereaux, C., Rossignol, M., Gadella, T.W.J., Imberty, A., Lefebvre, B., Cullimore, J.V. 2011. Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. J Biol Chem 286: 11202-11210. 
     

     

  • Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Andres Martinez, E., Driguez, H., Bécard, G. and J. Dénarié. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 469 : 58-63 
     

     

  • Mbengue, M., Camut, S., de Carvalho-Niebel, F., Deslandes, L., Froidure, S., Klaus-Heisen, D., Moreau, S., Rivas, S., Timmers, T., Hervé, C., Cullimore, J., Lefebvre, B. 2010. The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22: 3474-3488. 
     

     

  • Lefebvre, B., Timmers, T., Mbengue, M., Moreau, S., Hervé, C., Tóth, K., Bittencourt-Silvestre, J., Klaus, D., Deslandes, L., Godiard, L., Murray, J.D., Udvardi, M.K., Raffaele, S., Mongrand, S., Cullimore, J., Gamas, P., Niebel, A. and Ott, T. 2010. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci U S A. 107: 2343-2348.
     

     

  • Arrighi, J.F., Godfroy, O., de Billy, F., Saurat, O., Jauneau, A., Gough, C. 2008. The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection. Proc Natl Acad Sci U S A. 105:9817-9822. 
     

     

  • Lefebvre, B., Furt, F., Hartmann, M.A., Michaelson, L.V., Carde, J.P., Sargueil-Boiron, F., Rossignol, M., Napier, J.A., Cullimore, J., Bessoule, J.J., Mongrand, S. 2007. Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Phys. 144:402-418. 
     

     

  • Hogg, B.V., Cullimore, J.V., Ranjeva, Bono, J.J. 2006. The DMI1 and DMI2 early symbiotic genes of Medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol. 140:365-73. 
     

     

  • Mulder, L., Lefebvre, B., Cullimore, J.V., Imberty, A. 2006. LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modelling and docking of chitooligosaccharides and Nod factors. Glycobiology 16: 801-809. 
     

     

  • Oláh, B., Brière, C., Bécard, G., Dénarié, J., Gough, C. 2005. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44:195. 
     

     

  • Lévy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ané, J.M., Lauber, E., Bisseling, T., Dénarié, J., Rosenberg, C., Debellé, F. 2004. A Putative Ca²+ and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses. Science 303:1361-1364. 
     

     

  • Ané, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E., Ayax, C., Lévy, J., Debellé, F., Baek, J.M., Kalo, P., Rosenberg, C., Roe, B.A., Long, S.R., Dénarié, J., Cook, D.R. 2004. MedicagotruncatulaDMI1 required for bacterial and fungal symbioses in legumes. Science. 303:1364-1367. 
     

     

  • Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., Dénarié, J. 2000. Four genes of Medicagotruncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1666. 
     

     

  • Wais, R. J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R. V., Cook, D., Gough, C., Dénarié, J. and S. R. Long. 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci U S A., 97: 13407-13412.

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