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Les associations symbiotiques rhizobium-légumineuse sont finement régulées, et tant leur mise en place que leur fonctionnement peuvent être affectés par divers facteurs environnementaux. Notre groupe développe trois lignes de recherche sur les interactions rhizobium-légumineuse-environnement : i) la réponse générale aux stress des rhizobia ; ii) le monoxyde d’azote (NO) au cours de la symbiose rhizobium-légumineuse ; iii) l’influence de l’environnement biotique sur la symbiose rhizobium-légumineuse.
THÈMES DE RECHERCHE
La réponse générale au stress chez Sinorhizobium meliloti
Nous avons identifié le facteur sigma RpoE2 comme étant un régulateur majeur de la réponse générale au stress chez S. meliloti (Sauviac et al., 2007). En effet, en réponse à des conditions de stress ou de carence, RpoE2 contrôle l’expression de plus d'une centaine de gènes (Sallet et al., 2013), dont certains gènes de résistance au stress. Les orthologues de RpoE2 sont virtuellement universellement présents chez les alpha-Protéobactéries, où ils jouent des rôles variés dans l’adaptation aux stress et/ou la colonisation de l’hôte, ce qui suggère que ces facteurs sigma sont les analogues fonctionnels de sigmaS d’Escherichia coli. Nous avons caractérisé le mécanisme d’activation de RpoE2 en réponse au stress. Un modèle complexe a été proposé, impliquant 2 anti-sigma et 2 anti-anti-sigma agissant ensemble dans une cascade de partner-switching (Bastiat et al., 2010), sous le contrôle de diverses histidine kinases (Sauviac and Bruand, 2014).
Notre objectif actuel est de comprendre les fonctions physiologiques de la réponse RpoE2-dépendante. Ainsi, nous avons récemment montré que la réparation de cassures double-brin de l’ADN par NHEJ (Non homologous end-joining) était en partie contrôlée par RpoE2 chez S. meliloti (Dupuy et al., 2019).
Monoxyde d’azote (NO) et symbiose : synthèse et rôle du NO et de la réponse bactérienne associée
Le NO (monoxyde d'azote) est un des messagers de communication cellulaire parmi les plus étudiés chez les eucaryotes. Chez les animaux comme chez les plantes, le NO fait également partie de l’arsenal de défense de l’hôte contre l’infection par des bactéries pathogènes, et à ce titre, son rôle et celui de la réponse bactérienne associée sont très étudiés dans les interactions hôtes-pathogènes. Du NO est aussi présent dans le sol, et a également été détecté au cours des symbioses rhizobia-légumineuses. Cette molécule toxique peut donc représenter un stress pour les rhizobia, que ce soit en vie libre dans le sol, ou en symbiose avec les plantes. Il est donc intéressant de comprendre comment ces bactéries répondent à la présence de NO. Il est également important de comprendre le(s) rôle(s) du NO dans l’interaction symbiotique.
Nous avons montré, en réalisant des études transcriptomiques sur S. meliloti en culture, que le NO induisait l’expression d’une centaine de gènes. Nous avons découvert que plusieurs de ces gènes étaient impliqués directement ou indirectement dans la dégradation du NO (Meilhoc et al., 2010 ; Blanquet et al., 2015). Nous avons aussi montré que S. meliloti contribuait à la synthèse du NO présent dans les nodules de M. truncatula (Horchani et al., 2011) et avons identifié les voies de synthèse de cette molécule (Ruiz et al., 2019 ; Ruiz et al., 2021). Enfin nous avons montré que le NO jouait des rôles potentiellement différents à chaque étape de la symbiose (del Giudice et al., 2011 ; Cam et al., 2012) et avons identifié des cibles protéiques bactériennes du NO (Cazalé et al., 2020).
Notre objectif actuel est de continuer à caractériser les rôles du NO en symbiose et en particulier de déterminer si la production de NO par les bactéries joue un rôle spécifique au cours de cette interaction.
La symbiose rhizobium-légumineuse et son environnement biotique
L’environnement biotique des racines de légumineuse peut avoir des conséquences drastiques sur l’infection rhizobienne, sur l’organogénèse et sur le bon fonctionnement des nodosités et la persistance des rhizobia présentes en leur sein. Toutefois l’influence de la microflore rhizosphérique non-rhizobienne sur ces symbioses reste globalement très peu explorée. Nous cherchons à i) caractériser ces influences, ii) décrire les mécanismes qui les sous-tendent, iii) étudier l’impact de ces symbioses sur la vulnérabilité/résistance des plantes aux maladies.
Pour cela, nous travaillons principalement en utilisant des systèmes d’interactions tripartites Légumineuse-Rhizobium-Pathogène avec une part conséquente de l’effort actuel portée sur des systèmes biologiques impliquant des plantes cultivées.
Financements récents
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ANR STAYPINK 2016-2021 (Coord. C. Bruand)
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TULIP New Frontiers 2016-2018 (B. Gourion)
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INRA SPE 2016-2019 (B. Gourion)
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ANR Trolesinfidels 2018-2022 (B. Gourion)
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FRAIB ILUMINER 2018-2020 (J.-M. Couzigou LRSV / B. Gourion LIPME)
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FRAIB BIONOS 2019 (B. Ruiz)
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FRAIB RASPUTIN 2021 (T. Prévitali)
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ANR PATHOSYM 2021-2025 (B. Gourion LIPME / Coord. P. Ratet IPS2)
PUBLICATIONS
2023
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.
2022
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.
2021
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.
2020
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.
2019
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
2018
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.
2017
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
2016
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
2015
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.
2014
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.
2013
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.
2012
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
2011
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
2010
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.