top of page


Rhizobia, Legumes and Environment

Nom equipe
Thèmes de recherche

Rhizobium-legume symbiotic associations are tightly regulated, and both their development and function can be affected by various environmental factors. Our group develops three lines of research on rhizobium-legume-environment interactions: i) the general stress response of rhizobia; ii) nitric oxide (NO) during rhizobium-legume symbiosis; iii) the influence of the biotic environment on rhizobium-legume symbioses.


The general stress response in Sinorhizobium meliloti

We have identified the σ factor RpoE2 as a major regulator of the general stress response in S. meliloti (Sauviac et al. 2007). Indeed, in response to various stress or starvation conditions, RpoE2 controls the expression of more than a hundred genes (Sallet et al., 2013), including stress resistance genes. RpoE2 orthologues are virtually universally distributed among α-Proteobacteria where they play various roles in stress adaptation and/or host colonization, which suggests they are the long-searched functional analogs of Escherichia coli sigmaS. We have characterized the mechanism of activation of RpoE2 in response to stress. A complex model was proposed, involving 2 anti-sigma and 2 anti-anti-sigma factors working together in a partner-switching cascade (Bastiat et al. 2010), under the control of various histidine kinases (Sauviac and Bruand, 2014).


Our current goal is to better understand the physiological functions of the RpoE2-dependent response. In particular, we recently showed that DNA double-strand break repair by NHEJ (Non Homologous End-Joining) is partly controlled by RpoE2 in S. meliloti.

Nitric oxide (NO) and symbiosis: synthesis and role of NO and the associated bacterial response

NO (nitric oxide) is one of the most studied messengers of cellular communication in eukaryotes. In both animals and plants, NO is also part of the host defense arsenal against infection by pathogenic bacteria, and as such, its role and that of the associated bacterial response are widely studied in host-pathogen interactions. NO is also present in the soil, and has also been detected during rhizobia-legume symbiosis. This toxic molecule can therefore represent a stress for rhizobia, whether living free in the soil, or in symbiosis with legumes. It is therefore interesting to understand how these bacteria respond to the presence of NO. It is also important to understand the role (s) of NO in the symbiotic interaction.

We have shown, by performing transcriptomic studies on S. meliloti in culture, that NO induces the expression of a hundred genes. We discovered that several of these genes were directly or indirectly involved in the degradation of NO (Meilhoc et al., 2010; Blanquet et al., 2015). We have also shown that S. meliloti contributes to the synthesis of NO present in Medicago truncatula root nodules (Horchani et al., 2011) and have identified the synthetic pathways of this molecule (Ruiz et al., 2019; Ruiz et al., 2011). Finally, we have shown that NO plays potentially different roles at each stage of the symbiosis (del Giudice et al., 2011; Cam et al., 2012) and identified bacterial protein targets for NO (Cazalé et al., 2020 ).


Our current objective is to continue to characterize the roles of NO in symbiosis and in particular to determine whether the production of NO by bacteria plays a specific role during this interaction.


The rhizobium-legume symbiosis and its biotic environment


The biotic environment surrounding the legume roots can have drastic consequences on rhizobial infection, on nodule organogenesis, on the nodule functioning and on rhizobial persistence within the plant cells. However, the influence of non-rhizobial rhizospheric microflora on rhizobia-legume symbiosis remains largely unexplored. We aim at i) characterizing those influences, ii) describing the underlying molecular mechanisms, and iii) studying the impact of those symbioses on plant susceptibility/resistance against diseases. 

In order to tackle those questions, we use Legume– rhizobia-pathogen tripartite interaction systems with a significant part of our current effort being focused on biological systems involving crops.


Recent fundings

  • ANR STAYPINK 2016-2021 (Coord. C. Bruand)

  • TULIP New Frontiers 2016-2018 (B. Gourion)

  • INRA SPE 2016-2019 (B. Gourion)

  • ANR Trolesinfidels 2018-2022 (B. Gourion)

  • FRAIB ILUMINER 2018-2020 (JM. Couzigou LRSV/B. Gourion LIPME)

  • FRAIB BIONOS 2019 (B. Ruiz)

  • FRAIB RASPUTIN 2021 (T. Prévitali)

  • ANR PATHOSYM 2021-2025 (B. Gourion LIPME / Coord. P. Ratet IPS2)

Financements récents

  • ANR STAYPINK 2016-2021 (Coord. C. Bruand)

  • TULIP New Frontiers 2016-2018 (B. Gourion)

  • INRA SPE 2016-2019 (B. Gourion)

  • ANR Trolesinfidels 2018-2022 (B. Gourion)

  • FRAIB ILUMINER 2018-2020 (J.-M. Couzigou LRSV / B. Gourion LIPME)

  • FRAIB BIONOS 2019 (B. Ruiz)

  • FRAIB RASPUTIN 2021 (T. Prévitali)

  • ANR PATHOSYM 2021-2025 (B. Gourion LIPME / Coord. P. Ratet IPS2)



Berrabah F, Bernal G, Elhosseyn AS, El Kassis C, L'Horset R, Benaceur F, Wen J, Mysore KS, Garmier M, Gourion B, Ratet P, Gruber V. (2023) Insight into the control of nodule immunity and senescence during Medicago truncatula symbiosis. Plant Physiol.  2;191(1):729-746. doi: 10.1093/plphys/kiac505.

Gourion B. (2023) NCRs make the difference. Nature Plants doi: 10.1038/s41477-023-01346-8.


Sauviac L, Rémy A, Huault E, Dalmasso M, Kazmierczak T, Jardinaud MF, Legrand L, Moreau C, Ruiz B, Cazalé AC, Valière S, Gourion B, Dupont L, Gruber V, Boncompagni E, Meilhoc E, Frendo P, Frugier F, Bruand C. (2022) A dual legume-rhizobium transcriptome of symbiotic nodule senescence reveals coordinated plant and bacterial responses. Plant Cell Environ. 45(10):3100-3121. doi: 10.1111/pce.14389.

Ruiz B, Sauviac L, Brouquisse R, Bruand C, Meilhoc E. (2022) Role of Nitric Oxide of Bacterial Origin in the Medicago truncatula-Sinorhizobium meliloti Symbiosis Mol Plant Microbe Interact​. 35(10):887-892. doi: 10.1094/MPMI-05-22-0118-SC.

Soto MJ, Staehelin C, Gourion B, Cárdenas L, Vinardell JM. (2022) Editorial: Early signaling in the rhizobium-legume symbiosis. 

Front Plant Sci​. 19;13:1056830. doi: 10.3389/fpls.2022.1056830.

Jardinaud MF, Carrere S, Gourion B, Gamas P. (2022) Symbiotic Nodule Development and Efficiency in the Medicago truncatula Mtefd-1 Mutant is Highly Dependent on Sinorhizobium Strains. Plant Cell Physiol​. 24;pcac134. doi:10.1093/pcp/pcac134.


Gourion B, Ratet P. (2021) Avoidance of detrimental defense responses in beneficial plant-microbe interactions. Curr Opin Biotechnol. 70:266-272. doi: 10.1016/j.copbio.2021.06.008.

Benezech C, Le Scornet A, Gourion B. (2021) Medicago-Sinorhizobium-Ralstonia a model system to investigate pathogen triggered inhibition of nodulation Mol Plant Microbe Interact 34(5):499-503. doi: 10.1094/MPMI-11-20-0319-SC


Nicoud Q, Lamouche F, Chaumeret A, Balliau T, Le Bars R, Bourge M, Pierre F, Guérard F, Sallet E, Tuffigo S, Pierre O, Dessaux Y, Gilard F, Gakière B, Nagy I, Kereszt A, Zivy M, Mergaert P, Gourion B, Alunni B (2021) Bradyrhizobium diazoefficiens USDA110 Nodulation of Aeschynomene afraspera Is Associated with Atypical Terminal Bacteroid Differentiation and Suboptimal Symbiotic Efficiency. mSystems DOI: 10.1128/mSystems.01237-20

Ruiz B, Frostegård Å, Bruand C, Meilhoc E. (2021) Rhizobia: highways to NO. Biochem Soc Trans. doi: 10.1042/BST20200989.

Thibessard A, Bertrand C, Bartlett EJ, Doherty AJ, Bruand C, Leblond P, Lecointe F. (2021) Nonhomologous End-Joining in Bacteria.In: Jez Joseph (eds.) Encyclopedia of Biological Chemistry, 3rd Edition. vol. 4, pp. 289–295. Oxford: Elsevier.


Cazalé AC, Blanquet P, Henry C, Pouzet C, Bruand C, Meilhoc E. (2020) Tyrosine nitration of flagellins: a response of Sinorhizobium meliloti to nitrosative stress. Appl Environ Microbiol. 87(1):e02210-20. doi: 10.1128/AEM.02210-20.


Benezech C, Berrabah F, Jardinaud MF, Le Scornet A, Milhes M, Jiang G, George J, Ratet P, Vailleau F, Gourion B. (2020) Medicago-Sinorhizobium-Ralstonia Co-infection Reveals Legume Nodules as Pathogen Confined Infection Sites Developing Weak Defenses. Curr Biol. 30(2):351-358.e4. doi: 10.1016/j.cub.2019.11.066.


Benezech C, Doudement M, Gourion B. (2020) Legumes tolerance to Rhizobia is not always observed and not always deserved. Cell Microbiol. 22(1):e13124. doi: 10.1111/cmi.13124.


Ruiz B., Le Scornet A., Sauviac L., Rémy A., Bruand C., Meilhoc E. (2019) The nitrate assimilatory pathway in Sinorhizobium meliloti: Contribution to NO production. Frontiers in Microbiology 10:1526. doi: 10.3389/fmicb.2019.01526.


Baena I., Pérez-Mendoza D., Sauviac L., Francesch K., Martín M., Rivilla R., Bonilla I., Bruand C., Sanjuán J., Lloret J. (2019) A partner-switching system controls activation of mixed-linkage β-glucan synthesis by c-di-GMP in Sinorhizobium meliloti. Environ Microbiol. 21(9), 3379–3391. doi:10.1111/1462-2920.14624


Bertrand C., Thibessard A., Bruand C., Lecointe F., Leblond P. (2019) Bacterial NHEJ: a never ending story. Mol Microbiol. 111(5):1139-1151


Bruand C., Meilhoc E. (2019) NO in plants: pro or anti senescence. J Exp Bot. 70(17):4419-4427


Berrabah, F., Ratet, P., Gourion B. (2019) Legume nodule: massive infection in the absence of defense induction. Mol Plant Microbe Interact 32(1):35-44.


Dupuy, P., Sauviac, L., Bruand, C. (2019) Stress-inducible NHEJ in bacteria: function in DNA repair and acquisition of heterologous DNA Nucleic Acid Research 47(3):1335-1349


Berrabah, F., Balliau, T., Aït-Salem, E-H., George, J., Zivy, M., Ratet, P., Gourion B. (2018) Control of the ethylene signaling pathway prevents plant defenses during intracellular accomodation of the rhizobia New Phytol 219(1):310-323.

Sang Y, Wang Y, Ni H, Cazalé AC, She YM, Peeters N, Macho AP. (2018) The Ralstonia solanacearum type III effector RipAY targets plant redox regulators to suppress immune responses. Mol Plant Pathol 19(1):129-142.

Gourion, B., Alunni, B. (2018) Strain-specific symbiotic genes: a new level of control in the intracellular accommodation of rhizobia within legume nodule cells. Mol Plant Microbe Interact 31(3):287-288.


Dupuy, P., Gourion, B., Sauviac, L., Bruand, C. (2017) DNA double-strand break repair is involved in desiccation resistance of Sinorhizobium meliloti, but is not essential for its symbiotic interaction with Medicago truncatula. Microbiology 163: 333-342

Lonjon F, Lohou D, Cazalé AC, Büttner D, Ribeiro BG, Péanne C, Genin S, Vailleau F. (2017) HpaB-Dependent Secretion of Type III Effectors in the Plant Pathogens Ralstonia solanacearum and Xanthomonas campestris pv. vesicatoria. Sci Rep7(1):4879

Brusamarello-Santos LC, Gilard F, Brulé L, Quilleré I, Gourion B, Ratet P, Maltempi de Souza E, Lea PJ, Hirel B. (2017) Metabolic profiling of two maize (Zea mays L.) inbred lines inoculated with the nitrogen fixing plant-interacting bacteria Herbaspirillum seropedicae and Azospirillum brasilense. PLoS One 12(3):e0174576


Alunni, B., Gourion, B. (2016) Terminal bacteroid differentiation in the legume-rhizobium symbiosis: nodule-specific cysteine-rich peptides and beyond. New Phytol 211(2):411-7


Blanquet, P., Silva, L., Catrice, O., Bruand, C., Carvalho, H., and Meilhoc, E. (2015) Sinorhizobium meliloti controls NO-mediated post-translational modification of a Medicago truncatula nodule protein. Mol Plant Microbe Interact 28(12):1353-63 Full text

Sauviac, L., Bastiat, B., and Bruand, C. (2015) The general stress response in alpha-rhizobia (review) In Biological Nitrogen Fixation, F.J. de Bruijn (ed), Wiley-Blackwell (Hoboken, NJ, USA), p. 405-414.

Meilhoc, E., Boscari, A., Brouquisse, R., and Bruand, C. (2015) Multifaceted roles of nitric oxide in legume-rhizobium symbioses (review) In Biological Nitrogen Fixation, F.J. de Bruijn (ed), Wiley-Blackwell (Hoboken, NJ, USA), p. 637-648.

Vriezen, J.A.C., and de Bruijn, F.J. (2015) Appearance of membrane compromised, viable but not culturable and culturable rhizobial cells as a consequence of desiccation. In Biological Nitrogen Fixation, F.J. de Bruijn (ed), Wiley-Blackwell (Hoboken, NJ, USA), p. 977-989.

de Bruijn, F.J. (2015) The quest for biological nitrogen fixation in cereals : a perspective and prospective. In Biological Nitrogen Fixation, F.J. de Bruijn (ed), Wiley-Blackwell (Hoboken, NJ, USA), p. 1089-1101.

de Bruijn, F.J. (2015) Biological Nitrogen Fixation, Vol 1 and 2, FJ de Bruijn (ed), Wiley-Blackwell (Hoboken, NJ, USA)

de Bruijn, F.J. (2015) Biological nitrogen fixation. In Principles of Plant-Microbe interactions, Microbes for sustainable agriculture, B. Lugtenberg (ed), Springer International Publishing, Switzerland.


Sauviac, L., and Bruand, C. (2014) A putative bifunctional histidine kinase/phosphatase of the HWE family exerts positive and negative control on the Sinorhizobium meliloti general stress response. J Bacteriol 196:2526-35.

Roux, B., Rodde, N., Jardinaud, M.F., Timmers, T., Sauviac, L., Cottret, L., Carrère, S., Sallet, E., Courcelle, E., Moreau, S., Debellé, F., Capela, D., de Carvalho-Niebel, F., Gouzy, J., Bruand, C., and Gamas, P. (2014) An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J 77:817-837.


Savka, M.A., Dessaux, Y., McSpadden Gardener, B.B., Mondy, S., Kohler, P.R.A., de Bruijn, F.J., and Rossbach, S. (2013) The “biased rhizosphere” concept and advances in the omics era to study bacterial competitiveness and persistence in the phytosphere. In Molecular Microbial Ecology of the Rhizosphere (de Bruijn, F.J., ed), John Wiley & Sons, Inc., Hoboken, NJ, USA., 1147-1161

Boscari, A., Meilhoc, E., Castella, C., Bruand, C., Puppo, A., and Brouquisse, R. (2013) Which role for nitric oxide in symbiotic N2-fixing nodules: toxic by-product or useful signaling/metabolic intermediate? Front Plant Sci 4:384. Review

Vriezen, J.A., de Bruijn, F.J., and Nüsslein, K. (2013) Identification and characterization of a NaCl-responsive genetic locus involved in survival during desiccation in Sinorhizobium meliloti. Appl Environ Microbiol 79:5693-700.

Meilhoc, E., Blanquet, P., Cam, Y., and Bruand, C. (2013) Control of NO level in rhizobium-legume root nodules: Not only a plant globin story. Plant Signal Behav 8:e25923.

Sallet, E., Roux, B., Sauviac, L., Jardinaud, M.-F., Carrère, S., Faraut, T., de Carvalho-Niebel, F., Gouzy, J., Gamas, P., Capela, D., Bruand, C., and Schiex, T. (2013) Next-generation annotation of prokaryotic genomes with EuGene-P: application to Sinorhizobium meliloti 2011. DNA Res 20:339-354.

de Bruijn, F.J. (2013) Molecular Microbial Ecology of the Rhizosphere, Volume I & II. (de Bruijn, F.J., ed), John Wiley & Sons, Inc., Hoboken, NJ, USA.


Bastiat, B., Sauviac, L., Picheraux, C., Rossignol, M., and Bruand, C. (2012) Sinorhizobium meliloti sigma factors RpoE1 and RpoE4 are activated in stationary phase in response to sulfite. PLoS One 7:e50768.

Cam, Y., Pierre, O., Boncompagni, E., Hérouart, D., Meilhoc, E., and Bruand, C. (2012) Nitric oxide (NO): a key player in the senescence of Medicago truncatula root nodules. New Phytol 196: 548-560. Full text

Vriezen, J.A., de Bruijn, F.J., and Nüsslein, K.R. (2012) Desiccation induces viable but non-culturable cells in Sinorhizobium meliloti 1021. AMB Express 2:6. Full text 


Meilhoc, E., Boscari, A., Bruand, C., Puppo, A., and Brouquisse, R. (2011) Nitric oxide in legume-rhizobium symbiosis. Plant Sci 181:573-581. Review Full text

de Bruijn, F.J. (2011) Handbook of Molecular Microbial Ecology I: Metagenomics and complementary approaches & II: Metagenomics in different habitats (de Bruijn, F.J., ed), John Wiley & Sons, Inc., Hoboken, NJ, USA.

del Giudice, J., Cam, Y., Damiani, I., Fung-Chat, F., Meilhoc, E., Bruand, C., Brouquisse, R., Puppo, A., and Boscari, A. (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405-417. Full text

Horchani, F., Prevot, M., Boscari, A., Evangelisti, E., Meilhoc, E., Bruand, C., Raymond, P., Boncompagni, E., Aschi-Smiti, S., Puppo, A., and Brouquisse, R. (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatulanitrogen-fixing nodules. Plant Physiol 155: 1023-1036. Full text


Bastiat, B., Sauviac, L., and Bruand, C. (2010) Dual control of Sinorhizobium meliloti RpoE2 sigma factor activity by two PhyR-type two-component response regulators. J Bacteriol 192: 2255-2265. Full text 

Meilhoc, E., Cam, Y., Skapski, A., and Bruand, C. (2010) The response to nitric oxide of the nitrogen-fixing symbiont Sinorhizobium meliloti. Mol Plant Microbe Interact 23: 748-759. Full text


Antérieur à 2010

Rossbach, S., Mai, D.J., Carter, E.L., Sauviac, L., Capela, D., Bruand, C., and de Bruijn, F.J. (2008) Response of Sinorhizobium meliloti to elevated concentrations of cadmium and zinc. Appl Environ Microbiol 74: 4218-4221.  


Vriezen, J.A., de Bruijn, F.J. and Nussslein K. (2007) Responses of rhizobia to dessication in relation to osmotic stress, oxygen and temperature.  Appl Environ Microbiol 72, 3451-3459.  


Rossbach, S., de Bruijn, F.J., (2007) Transposon mutagenesis.  In: Methods for General and Molecular Microbiology., Ed. C.A Reddy, American Society for Microbiology, Washington, DC, PP. 684-708

Sauviac, L., Philippe, H., Phok, K., and Bruand, C. (2007) An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. J Bacteriol 189: 4204-4216.  


Vriezen, J.A.C., Wopereis, J.,  de Bruijn, F.J., Nusslein, K. (2006) Dessication responses of    Sinorhizobium meliloti USDA 1021 in relation to growth phase, temperature, chloride and sulfate availability.  (2006) Lett Appl Microbiol 42, 172-178.  


de Bruijn, F.J., Rossbach, S., Bruand, C., and Parrish, J.R. (2006) A highly conserved Sinorhizobium meliloti operon is induced microaerobically via the FixLJ system and by nitric oxide (NO) via NnrR. Environ Microbiol  8: 1371-1381.  


Bobik, C., Meilhoc, E., and Batut, J. (2006) FixJ: a major regulator of the oxygen limitation response and late symbiotic functions of Sinorhizobium meliloti. J Bacteriol 188: 4890-4902.  


Capela, D., Filipe, C., Bobik, C., Batut, J., and Bruand, C. (2006) Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection. Mol Plant Microbe Interact19: 363-372.  

bottom of page