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Nom equipe
Thèmes de recherche

RESEARCH THEMES

Signalling Mechanisms in Symbiosis

The SMS group studies the mechanisms of symbiotic signalling that underlie establishment of the Arbuscular Mycorrhizal (AM) symbiosis and the Rhizobium-Legume (RL) symbiosis. These plant-microbe interactions can provide major benefits to plants, notably improved nutrition and improved resistance to moderate biotic and abiotic stress, and are therefore of foremost agronomic and ecological importance. We aim to understand the molecular and genetic mechanisms underlying symbiosis establishment, which should contribute to future strategies for reducing fertiliser and pesticide use through maintaining symbiosis capacity in changing climatatic conditions.

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Symbiosis establishment involves microbially produced signalling molecules and modifications to plant root development. The best studied rhizobial and AM fungal signals are lipo-chitooligosaccharides (LCOs), which are essential for establishing many Rhizobial symbioses and which  influence establishment of the AM symbiosis and root development. LCOs are also produced by non-symbiotic fungi, and can interfere with plant immunity against pathogens.  

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For many years, we have been studying the perception of Rhizobial LCOs, called Nod factors (NFs), and how they control root nodulation and infection in legumes.  This has led to studies on the signalling mechanisms implicated in symbiosis establishment,  how host specificity is controlled and which pathways are controlled by LCOs to influence root development and how they cross-talk with auxin signalling and homeostasis. We are also studying how AM fungi can influence endodermal root barrier permeability and nutrient exchange.

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Our model plants.

Left, Medicago truncatula and right, pea (Pisum sativum).

Previously, we identified Medicago truncatula Lysin-motif receptor-like kinases (LysM-RLKs), controlling symbiosis and/or LCO perception. For example, MtNFP is essential for NF perception and for nodulation, while MtLYK9 controls the AM symbiosis (refs). MtNFP and MtLYK9 also control immunity against pathogens, and these dual roles likely involve cellular redox state regulation. Furthermore, the NF-stimulation of lateral root formation in M. truncatula is dependent on MtNFP, and we have shown that LCOs potentiate an auxin effect, at both the phenotypic level of lateral root formation and the level of gene expression.

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Arbuscular mycorrhizal (AM) fungi and rhizobial bacteria produce lipo-chitooligosaccharidic (LCO) signals, Myc-LCOs and Nod factors, which are recognised by plant lysin-motif receptor-like kinases (LysM-RLKs), leading to mycorrhization, nodulation and changes in root development.

            To better understand symbiotic signalling mechanisms, and how pathways of root development and immunity are recruited and controlled for nodulation and mycorrhization, as well as how they are coordinated and influenced by the environment, we have 4main research themes that all focus on model and cultivated legume plants, mainly M. truncatula and pea:

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(1) Deciphering the links between symbiosis, redox state, immunity and the environment;

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(2) Understanding the influence of microbial signals on root development and symbiosis;

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(3) Characterising plant and bacterial components controlling host specificity and partner choice in the RL symbiosis;

 

(4) Understand how the deposition of endodermal barriers is coordinated with the establishment of endosymbiosis

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(1) Deciphering the links between symbiosis, redox state, immunity and the environment

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PIs : Clare Gough et Nicolas Pauly

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Reactive oxygen species (ROS) are a universal signalling messenger widely known for their roles in plant-microbe interactions, abiotic stress responses and plant developmental processes. As such, ROS are key molecules involved at the crossroads of perception of different stress factors, and regulation of both specific and general plant responses to environmental stimuli. RBOH genes, which encode NADPH oxygenases responsible for ROS production, belong to a versatile multigenic family, with members controlling different aspects of plant-microbe interactions, abiotic stress resistance and plant development.

In Medicago truncatula, ROS are involved in rhizobial infection and nodule functioning. Furthermore, NFs can inhibit ROS induction by a pathogen. This and other data indicate that there are interconnections between the symbiotic control of ROS production and immunity. We hypothesise that the symbiotic and immune-related roles of MtNFP and MtLYK9 involve redox regulation, and that immunity-related mechanisms are controlled and exploited for symbiosis.

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To address these questions, we aim first to better understand the role of ROS in early steps of NF signalling and nodulation. For this, we are using MtRBOH mutants and different methods of ROS detection, including redox biosensors to study the spatio-temporal dynamics of ROS production in planta.

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Principal and in planta use of a ROS biosensor. A, The Grx1-roGFP construct emits fluorescence as a function of its oxidized/reduced state, enabling ratiometric measurements. B and C, Preliminary results showing M. truncatula WT roots stably expressing the biosensor reveal differential oxidized states in infected root hairs (B) and a mature nodule section (C). The scale bar indicates highly reduced (blue) towards highly oxidized (yellow) states.

In collaboration with C. Jacquet (LRSV, Toulouse), we are also studying the role of ROS in a pathogenic context. These tools and results are combined with symbiotic plant mutants to decipher the roles of MtNFP and MtLYK9 in controlling ROS production for symbiosis and immunity. We are also using a transcriptomic approach and identifying new MtNFP interacting proteins to understand the dual role of MtNFP in nodulation and immunity.

A related objective is to understand how environmental abiotic stress affects symbiosis, and investigate whether symbiotic genes keep in check environmental abiotic stress-type responses of the plant that occur during symbiotic infection.

This work is part of an ANR project (DUALITY), with 3 partners: C. Jacquet, (LRSV, Toulouse), A. Boscari (Institut Sophia Agrobiotech, Nice) and J.F. Arrighi (IRD, Montpellier).

(2) Understanding the influence of microbial signals on root development and symbiosis

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PI : Sandra Bensmihen

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Soil microbes are more and more emerging as major determinants of root development plasticity. Our main research interests are in understanding how lipo-chitooligosaccharide molecules (LCOs), produced by symbiotic microbes such as rhizobia or arbuscular mycorrhizal fungi, can influence plant root development and more specifically the formation of new lateral roots (LR) (see Figure below).

We are mostly working on the model legume Medicago truncatula but are also interested in other legume plants (such as pea) and non legumes (such as the model monocot Brachypodium distachyon (Buendia et al., 2019)).

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LCO treatment leads to the formation of new lateral roots in Medicago truncatula

We showed that LCOs potentiate auxin action on LR formation and gene expression in Medicago and Brachypodium (Herrbach et al., 2017 ; Buendia et al., 2019) and are now interested in better understanding the molecular mechanisms by which LCOs potentiate auxin responses and how does this control LRF stimulation, nodulation and mycorrhization.

 

To unravel these molecular mechanisms, we are using a variety of approaches, ranging from natural genetic variation among M. truncatula natural accessions to perform Genome Wide Association Studies (GWAS, in collaboration with M. Bonhomme and C. Jacquet, LRSV) to transcriptomics, cellular and pharmacological approaches.

 

To enable more efficient screening of root phenotypes, we are developping high throughput root phenotyping together with the Toulouse Plant Microbe Phenotyping (TPMP) platform facility, on-site.

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(left) Examples of Medicago truncatula natural accessions showing contrasted root architecture

(right) Root phenotyping robot at TPMP and root images segmentation.

We are also interested in the molecular mechanisms governing more generally LR formation in Medicago (Herrbach et al., 2014), the specificities of LRF in legumes and how does this relate to nodule organogenesis. To address this, we are currently using both reverse genetics and comparative transcriptomics approaches (collaboration with the team of T. Beeckman, VIB Ghent, Belgium).

 

Together with M. Libault (University of Nebraska, USA) and Jean-Malo Couzigou (LRSV, Toulouse) we are setting up single cell transcriptomics approaches in Medicago.  We also continue to develop tissue-specific tools to address cell autonous and non cell automonous effect of LCO actions (Rival et al., 2012 ; Sevin-Pujol et al., 2017).

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Expression pattern of LaSCR1 :GUS in M. truncatula roots and nodules (From Sevin-Pujol et al., 2017) (GUS staining appears in blue, counter staining is ruthenium red)

 (3) Host specificity and Partner Choice in the Legume-Rhizobium Symbiosis

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PIs: Frédéric Debellé and Julie Cullimore

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Although it has been known for decades that different legume species form nitrogen-fixing symbiosis with different Rhizobial strains, the mechanisms involved are still far from being elucidated. Rhizobial Nod factors (NFs) and their perception by legume LysM-RLKs is the key first layer of control of partner choice.

Currently we are continuing our multi-disciplinary approach (genetics, biochemistry, cell biology) on the model Medicago-Sinorhizobium symbiosis firstly to identify new plant genes involved in partner specificity and secondly to understand the role of NFs and Lysin-motif receptor-like kinases (LysM-RLKs) in determining the ability of two diverse Medicago truncatula genotypes to nodulate with different Rhizobial mutant and natural strains.

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On pea, a legume crop that is important in France, we are investigating how LysM-RLKs are involved in the selection by the legume host of its Rhizobial partners in mixed Rhizobial inocula. This work is part of a larger project (GRASP) funded by the ANR and coordinated by V. Bourion (INRAE, Dijon), aimed at understanding the mechanisms of partner selection in the environment. Such knowledge could lead to improving the ability of legumes to select and nodulate with more efficient Rhizobium strains and thus to an improvement in symbiotic nitrogen fixation in an agronomic context.

 

We are also part of a collaboration, coordinated by J.-F. Arrighi (LSTM, Montpellier), to understand the mechanisms by which some legume species have evolved to form nitrogen-fixing symbioses with Rhizobia, independent of NF signaling.

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(4) Understand how the deposition of endodermal barriers is coordinated with the establishment of endosymbiosis

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PI: Guilhem Reyt

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Plant roots are vital for survival and growth as they regulate the intake of water and nutrients from the soil along with their transport to the shoot. Roots develop specific diffusional barriers in the endodermis, a cell layer separating the inner parts from the external parts of the root. These barriers balance uptake of nutrients, water, and interactions with soil microorganisms. Roots are also able to form symbioses with beneficial microbes such as arbuscular mycorrhizal fungi or nitrogen-fixing rhizobial bacteria to assist in nutrient acquisition. These symbioses form specific structures in the outer parts of the roots where reciprocal exchange of nutrients occurs. However, it is still unclear how the transfer of nutrients occurs between these symbiotic structures and the vascular tissues.

 

We aim to understand how the deposition of root barriers is coordinated with the arbuscular mycorrhizal and rhizobial symbioses, and how this impacts plant nutrition in the genetic model legume Medicago truncatula. We are developing imaging techniques to describe how root barrier deposition is coordinated with the formation of symbiotic structures. We are using symbiotic mutants and single-cell transcriptomic analysis to reveal how the symbiotic pathway controls endodermal differentiation. Finally, we are investigating how impairments in root barrier deposition impact the formation of symbiotic structures and plant nutrition. Altogether, this should lead to the identification of regulatory mechanisms controlling the efficiency of symbioses, first step for the rational manipulation of plant-microbe interactions to enhance plant productivity.

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A. Lignin staining in a nodule. Maximum intensity projection of confocal microscopy images of a whole nodule (Left) and transverse plane (Right). Lignin was visualized using basic fuchsin (Cyan) and bacteroids were stained with WGA-488 (Alexa Fluor 488 conjugate of Wheat Germ Agglutinin, Left only).

B. Suberin staining in a root colonized by arbuscular mycorrhizal fungi (AMF). Maximum intensity projection of mycorrhized roots stained with Nile Red for Suberin (red) and WGA-488 for AMF (cyan). The maximum intensity projections are from z-stacks including the top endodermal and the above-located cortical cells. Fungal structures are located above the endodermal cells. Upper image shows a partially suberised endodermis and fungal structures. Lower image shows an endodermal passage cell (see asterisk) located next to an arbuscule. Arrows indicate arbuscules.

thème (1)
thème (2)
Thème 3
Theme 4

MEMBERS

Membres
Anciens membres
Publications

PUBLICATIONS

  • Bouchiba Y, Esque J, Cottret L, Maréchaux M, Gaston M, Gasciolli V, Keller K, Nouwen N, Gully D, Arrighi J-F, Gough C, Lefebvre B, Barbe S, Bono J-J. (2022). An integrated approach reveals how lipo-chitooligosaccharides interact with the lysin motif receptor-like kinase MtLYR3. Protein Science 2022;31:e4327. https://doi.org/10.1002/pro.4327

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  • Bonhomme M, Bensmihen S, André O, Amblard E, Garcia M, Maillet F, Puech-Pagès V, Gough C, Fort S, Cottaz S, Bécard G, Jacquet C. (2021).  Distinct genetic basis for root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins. J. Exp. Botany DOI: 10.1093/jxb/erab096/6155747

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  • 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

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  • 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.

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  • 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
     

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

  • 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
     

  • 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. 
     

  • 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 

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  • 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). 

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  • 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. 

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  • 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. 

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  • 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. 
     

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  • 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. 

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  • 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. 

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  • 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. 

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  • 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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