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ENOD

ENDOSYMBIOTIC INFECTION AND NODULE DEVELOPMENT

Fernanda de Carvalho-Niebel
Andreas Niebel

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Most terrestrial plants have the ability to establish endosymbiotic associations with microbes to acquire essential nutrients for growth. Remarkable associations with nitrogen-fixing soil bacteria form specialized root organs, the nodules, hosting bacterial symbionts in an optimal environment for nitrogen fixation and thus the sustainable and biological production of nitrogen compounds. Our team focuses on the study of these sustainable nitrogen-fixing endosymbioses in Fabales (legume) plant species, interacting symbiotically with bacteria collectively called rhizobia. Our research focus on understanding the mechanisms underlying nodule development and coordinated bacterial colonization in legumes. Our specific objectives are to dissect (1) the cellular mechanisms regulating rhizobia infection and (2) transcriptional and epigenetic mechanisms behind nodule development. Within this framework, we use complementary model legumes (notably Medicago truncatula) and employ a range of approaches: molecular biology, reverse genetics, transcriptomics, (epi)genomics and microscopy methods, including cutting-edge live cell imaging techniques.

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RESEARCH THEMES

1. Regulation and dynamics of rhizobial infection

Host-controlled intracellular bacteria accommodation is essential for the establishment of a functional nodule. In this process, the plant orchestrates synchronized developmental programs necessary for the rewiring of plant cells  for nodule organogenesis and bacterial entry, which in most legume species occurs via elaborate tubular structures, called infection threads. The development of these structures by polar growth is essential to ensure the progressive colonization of root cells and, ultimately, of the nodule primordium. Their construction is closely synchronized with the development of the nodule and involves cell-specific symbiotic reprogramming of plant cells. Major players in these processes have only recently started to emerge. Our main scientific objectives are to identify the cellular mechanisms and key molecular players underlying the development of the infection thread and the associated cellular reprogramming. In this context, we are combining functional genomics and microscopy-driven approaches (notably live cell imaging) to (i) identify the main plant regulators of this process and (ii) track live cell reprogramming and cross talk between plant and bacterial partners during  infection thread development.

 

Contact :

Fernanda de Carvalho-Niebel (DR CNRS), Joëlle Fournier (CR CNRS) 

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Collaborations:
 

A. Becker (SYNMIKRO, Marburg, Germany); Mr. Marín  (LMU, Munich, Germany); E. Larrainzar (University of Navarra, Pamplona, Spain); Peter Kaló (NAIK, Gödöllő, Hungary); S. Radutoiu (Aarhus University, Denmark); J. Keller (Max-Planck Institute, Jena, Germany); J.F. Arrighi (PHIM, Montpellier); F. Cartielaux, V. Hocher & S.Svistoonoff  (PHIM, Montpellier); E. Boncompagni (ISA, Sophia-Antipolis); N. Frei-Dit-Frey/P.M. Delaux (LRSV, Toulouse); E. Jamet (LRSV, Toulouse); G. Reyt (LIPME); D. Capela (LIPME).

Funding:
 

ANR-DFG PRCI Live Switch (2020-2024), INRAE-SPE CREPE (2020-2023);

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2. Transcription and epigenetic regulation of nodular development

Nodule development in legumes involves sequential phases of bacterial accommodation and differentiation into a functional nitrogen-fixing organ. These developmental switches involve major transcriptional reprogramming orchestrated by a variety of plant symbiotic transcription factors (TFs). We have identified key TFs that regulate different phases of nodule development and differentiation, including pioneer TFs, known to regulate developmental switches. These TFs act together with key epigenetic mechanisms to regulate the transcription of symbiotic genes. Our main objective is to elucidate their role and mode of action, as well as the associated molecular mechanisms allowing transcriptional reprogramming leading to nodule organogenesis. This includes the study of so-called symbiotic islands, genomic clusters of neighboring symbiotic genes that are co-regulated during nodulation. In this context, we are also investigating the role of a repertoire of epigenetic regulators and the 3D hxromatin architecture in the nodulation-associated transcriptional reprogramming.

Contact :

Andreas Niebel (DR CNRS), Matthias Benoit (CR INRAE)

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Collaborations:
 

F. Ariel (University of Santa Fe, Argentina); F. Blanco & E. Zanetti (University of La Plata, Argentina); S. Sinharoy (National Institute of Plant Genome Research, New Delhi, India); M. Benhamed/M. Crespi/F. Frugier (IPS2, Paris-Saclay); F. Pontvianne (LGDP, Perpignan); M. Hanemian/F. Roux (LIPME), N. Frei-dit-Frey (LRSV); (B. Favery, S. Jaubert, ISA Nice).

 

Funding:

ANR PIOSYM (2020-2024), CNRS IRP LOCOSYM (2023-2027), INRAE SPE PhD Contract (2023-2026), Occitanie Region Emergence EpiSYMBIOSIS (2023-2026)

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MEMBERS

Thèmes de recherche
Membres
Regulation Dyn Inf
Transcription Epigénet

PUBLICATIONS

Publications (last 5 years)
 

  • 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 2022 Sep 24:pcac134. doi: 10.1093/pcp/pcac134.

  • Pecrix Y, Sallet E, Moreau S, Bouchez O, Carrere S, Gouzy J, Jardinaud MF, Gamas P. 2022. DNA demethylation and hypermethylation are both required for late nodule development in Medicago. Nat Plants. doi: 10.1038/s41477-022-01188-w. Online ahead of print. PMID: 35817824  https://rdcu.be/cRps3

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  • Jardinaud MF, Fromentin J, Auriac MC, Moreau S, Pecrix Y, Taconnat L, Cottret L, Aubert G, Balzergue S, Burstin J, Carrère S, Gamas P. 2022 . MtEFD and MtEFD2: two transcription factors with distinct neofunctionalization in symbiotic nodule development. Plant Physiol 2022 Apr 26:kiac177. doi: 10.1093/plphys/kiac177. Online ahead of print.                                                                                                        

  • Jiang S, Jardinaud MF, Gao J, Pecrix Y, Wen J, Mysore K, Xu P, Sanchez-Canizares C, Ruan Y, Li Q, Zhu M, Li F, Wang E, Poole PS, Gamas P, Murray JD. 2021 . NIN-like protein transcription factors regulate lehemoglobin genes in vegetable nodules. Science 374:625-628. https://www.science.org/doi/10.1126/science.abg5945                                                                                                                                                                                                                                          

  • Carrère S, Verdier J, Gamas P. 2021 . MtExpress, a Comprehensive and Curated RNAseq-based Gene Expression Atlas for the Model Legume Medicago truncatula. Plant Cell Physiol 62:1494-1500. https://doi.org/10.1093/pcp/pcab110

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  • Kirolinko C, Hobecker K, Wen J, Mysore KS, Niebel A, Blanco FA, Zanetti ME. 2021 . Auxin Response Factor 2 (ARF2), ARF3, and ARF4 Mediate Both Lateral Root and Nitrogen Fixing Nodule Development in Medicago truncatula. Front Plant Sci 12:659061. doi: 10.3389/fpls.2021.659061.  

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  • Shrestha A, Zhong S, Therrien J, Huebert T, Sato S, Mun T, Andersen SU, Stougaard J, Lepage A, Niebel A, Ross L, Szczyglowski K. 2021 . Lotus japonicus Nuclear Factor YA1, a nodule emergence stage-specific regulator of auxin signaling. New Phytol 229:1535-1552. doi: 10.1111/nph.16950.

     

  • Gavrin A, Rey T, Torode TA, Toulotte J, Chatterjee A, Kaplan JL, Evangelisti E, Takagi H, Charoensawan V, Rengel D, Journet EP, Debellé F, de Carvalho-Niebel F, Terauchi R, Braybrook S, Schornack S 2020 . Developmental Modulation of Root Cell Wall Architecture Confers Resistance to an Oomycete Pathogen. Curr Biol 30:4165-4176.e5. doi: 10.1016/j.cub.2020.08.011. Epub 2020 Sep 3.

     

  • 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 30:351-358.e4. doi: 10.1016/j.cub.2019.11.066.
     

  • 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. doi: 10.1111/tpj.14625.

     

  • Chabaud M, Fournier J, Brichet L, Abdou-Pavy I, Imanishi L, Brottier L, Pirolles E, Hocher V, Franche C, Bogusz D, Wall LG, Svistoonoff S, Gherbi H, Barker DG. 2019 . Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species. PLoS One 14:e0223149. doi: 10.1371/journal.pone.0223149.

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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 pii: pcz177. doi: 10.1093/pcp/pcz177.

     

  • Liu CW, Breakspear A,  Stacey N, Findlay K, Nakashima J, Ramakrishnan K, Liu M, Xie F, Endre G, de Carvalho-Niebel F, Oldroyd GED, Udvardi MK, Fournier J, Murray JD. 2019 . A protein complex required for polar growth of rhizobial infection threads. Nat Comm 10:2848-2864. doi: 10.1038/s41467-019-10029-y.

     

  • Tan S, Debellé F, Gamas P, Frugier F, Brault M. 2019 . Diversification of cytokinin phosphotransfer signaling genes in Medicago truncatula and other vegetable genomes.  BMC Genomics 20:373. doi: 10.1186/s12864-019-5724-z.

     

  • Liu CW, Breakspear A, Guan D, Cerri MR, Jackson K, Jiang S, Robson F, Radhakrishnan GV, Roy S, Bone C, Stacey N, Rogers C, Trick M, Niebel A, Oldroyd GED, de Carvalho-Niebel F , Murray JD. 2019 . NIN Acts as a Network Hub Controlling a Growth Module Required for Rhizobial Infection. Plant Physiol 179:1704-1722. doi: 10.1104/pp.18.01572.  
     

  • Pecrix Y, Staton SE, Sallet E, Lelandais-Brière C, Moreau S, Carrère S, Blein T, Jardinaud MF, Latrasse D, Zouine M, Zahm M, Kreplak J, Mayjonade B, Satgé C, Perez M, Cauet S, Marande W, Chantry-Darmon C, Lopez-Roques C,  Bouchez O, Bérard A, Debellé F, Muños S, Bendahmane A, Bergès H, Niebel A, Buitink J, Frugier F, Benhamed M, Crespi M, Gouzy J, Gamas P. 2018 . Whole-genome landscape of Medicago truncatula symbiotic genes. Nat Plants 4:1017-1025. doi: 10.1038/s41477-018-0286-7.  
     

  • Gaudioso-Pedraza R, Beck M, Frances L, Kirk P, Ripodas C, Niebel A, Oldroyd GED, Benitez-Alfonso Y, de Carvalho-Niebel F. 2018 . Callose-Regulated Symplastic Communication Coordinates Symbiotic Root Nodule Development.  Curr Biol 28:3562-3577 doi:10.1016/j.cub.2018.09.031.
     

  • Roux B, Rodde N, Moreau S, Jardinaud MF, Gamas P. 2018 . Laser Capture Micro-Dissection Coupled to RNA Sequencing: A Powerful Approach Applied to the Model Legume Medicago truncatula in Interaction with Sinorhizobium meliloti. Methods Mol Biol 1830:191-224. doi: 10.1007/978-1-4939-8657-6_12.

     

  • Fournier J, Imanishi L, Chabaud M, Abdou-Pavy I, Genre A, Brichet L, Lascano HR,  Muñoz N, Vayssières A, Pirolles E, Brottier L, Gherbi H, Hocher V, Svistoonoff S, Barker D, Wall LG. 2018 . Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization. New Phytol 219: 1018-1030. doi:10.1111/nph.15216

     

  • Kelner A, Leitão N, Chabaud M, Charpentier M, de Carvalho-Niebel F. 2018 . Dual Color Sensors for Simultaneous Analysis of Calcium Signal Dynamics in the Nuclear and Cytoplasmic Compartments of Plant Cells. Front Plant Sci 9:245. doi: 10.3389/fpls.2018.00245. eCollection.
     

  • Subrahmaniam HJ, Libourel C, Journet EP, Morel JB, Muños S, Niebel A, Raffaele S, Roux F. 2018 . The genetics underlying natural variation of plant-plant interactions, a beloved but forgotten member of the family of biotic  interactions. Plant J 93:747-770. doi: 10.1111/tpj.13799.

     

  • Rembliere C, Fournier J,  by Carvalho-Niebel F, Chabaud M. 2018 . A simple Agrobacterium tumefaciens-mediated transformation method for rapid transgene expression in Medicago truncatula root hairs. Plant Cell Tiss Organ Cult 132:181–190.

     

  • Sevin-Pujol A, Sicard M, Rosenberg C, Auriac MC, Lepage A, Niebel A, Gough C, Bensmihen S. 2017 . Development of a GAL4-VP16/UAS trans-activation system for tissue specific expression in Medicago truncatula. PLoS One . 12:e0188923. doi: 10.1371/journal.pone.0188923.
     

  • Gamas P, Brault M, Jardinaud MF, Frugier F. 2017 . Cytokinins in Symbiotic Nodulation: When, Where, What For? Trends Plant Sci 22:792-802. doi:10.1016/j.tplants.2017.06.012.  
     

  • Martin FM, Uroz S, Barker DG. 2017 . Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. Science 356(6340). pii: eaad4501. doi: 10.1126/science.aad4501.  
     

  • Cerri MR, Wang Q, Stolz P, Folgmann J, Frances L, Katzer K, Li X, Heckmann AB, Wang TL, Downie JA, Klingl A, de Carvalho-Niebel F, Xie F, Parniske M. 2017 . The ERN1 transcription factor gene is a target of the CCaMK/CYCLOPS complex and controls rhizobial infection in Lotus japonicus. New Phytol 215:323-337. doi: 10.1111/nph.14547.
     

  • Carotenuto G, Chabaud M, Miyata K, Capozzi M, Takeda N, Kaku H, Shibuya N, Nakagawa T, Barker DG, Genre A. 2017 . The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling. New Phytol 214:1440-1446. doi: 10.1111/nph.14539.  
     

  • Barker DG, Chabaud M, Russo G, Genre A. 2017 . Nuclear Ca(2+) signaling in arbuscular mycorrhizal and actinorhizal endosymbioses: on the trail of novel underground signals. New Phytol 214:533-538. doi: 10.1111/nph.14350.   
     

  • Ribeiro CW, Baldacci-Cresp F, Pierre O, Larousse M, Benyamina S, Lambert A, Hopkins J, Castella C, Cazareth J, Alloing G, Boncompagni E, Couturier J, Mergaert P, Gamas P, Rouhier N, Montrichard F, Frendo P. 2017 .  Regulation of Differentiation of Nitrogen-Fixing Bacteria by Microsymbiont Targeting of Plant Thioredoxin s1. Curr Biol  27:250-256. doi: 10.1016/j.cub.2016.11.013.                                                                                                                                                                                                                                                                                                                                            
     

  • Rey T, Laporte P, Bonhomme M, Jardinaud MF, Huguet S, Balzergue S, Dumas B, Niebel A, Jacquet C. 2016. MtNF-YA1, A Central Transcriptional Regulator of Symbiotic Nodule Development, Is Also a Determinant of Medicago truncatula Susceptibility toward a Root Pathogen. Front Plant Sci 7:1837.                                                                                                                                                       

  • Zanetti ME, Rípodas C, Niebel A. 2016. Plant NF-Y transcription factors: Key players in plant-microbe interactions, root development and adaptation to stress. Biochim Biophys Acta doi: 10.1016/j.bbagrm.2016.11.007.  
     

  • Satgé C, Moreau S, Sallet E, Lefort G, Auriac MC, Remblière C, Cottret L, Gallardo K, Noirot C, Jardinaud MF, Gamas P. 2016. Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. Nat Plants 2:16166. doi: 10.1038/nplants.2016.166.  
     

  • Fonouni-Farde C, Tan S, Baudin M, Brault M, Wen J, Mysore KS, Niebel A, Frugier F, Diet A. 2016. DELLA-mediated gibberellin signaling regulates Nod factor signaling and rhizobial infection. Common Nat 7:12636. doi:10.1038/ncomms12636.  
     

  • 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, 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 170:2312-24. doi:10.1104/pp.15.01694.  
     

  • Boivin S, Kazmierczak T, Brault M, Wen J, Gamas P, Mysore KS, Frugier F. 2016. Different cytokinin CHK receptors regulate nodule initiation as well as later nodule developmental stages in Medicago truncatula. Plant Cell Approx 39:2198-2209. doi: 10.1111/pce.12779.   
     

  • Jardinaud MF, Boivin S, Rodde N, Catrice O, Kisiala A, Lepage A, Moreau S, Roux B, Cottret L, Sallet E, Brault M, Emery RJ, Gouzy J, Frugier F, Gamas P. 2016. A laser dissection -RNAseq analysis highlights the activation of cytokinin pathways by Nod factors in the Medicago truncatula root epidermis. Plant Physiol 171:2256-76. doi: 10.1104/pp.16.00711.
     

  • Cerri MR, Frances L, Kelner A, Fournier J, Middleton PH, Auriac MC, Mysore KS, Wen J, Erard M, Barker DG, Oldroyd GE, de Carvalho-Niebel F. 2016. The Symbiosis-Related ERN Transcription Factors Act in Concert to Coordinate Rhizobial Host Root Infection. Plant Physiol 171:1037-54. doi: 10.1104/pp.16.00230.
     

  • Chabaud M, Gherbi H, Pirolles E, Vaissayre V, Fournier J, Moukouanga D, Franche C, Bogusz D, Tisa LS, Barker DG, Svistoonoff S. 2016. Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209:86-93. doi: 10.1111/nph.13732.  
     

  • Vernié T, Kim J, Frances L, Ding Y, Sun J, Guan D, Niebel A, Gifford ML, de Carvalho-Niebel F, Oldroyd GE. 2015. The NIN Transcription Factor Coordinates Diverse Nodulation Programs in Different Tissues of the Medicago truncatula Root. Plant Cell27:3410-3424. doi: 10.1105/tpc.15.00461.  
     

  • Roux B, Bolot S, Guy E, Denancé N, Lautier M, Jardinaud MF, Fischer-Le Saux M, Portier P, Jacques MA, Gagnevin L, Pruvost O, Lauber E, Arlat M, Carrère S, Koebnik R, Noël LD . 2015. Genomics and transcriptomics of Xanthomonas campestris species challenge the concept of core type III effectome. BMC Genomics 16:975. doi: 10.1186/s12864-015-2190-0.  
     

  • Baudin M, Laloum T, Lepage A, Rípodas C, Ariel F, Frances L, Crespi M, Gamas P, Blanco FA, Zanetti ME, de Carvalho-Niebel F, Niebel A. 2015. A Phylogenetically Conserved Group of Nuclear Factor-Y Transcription Factors Interact to Control Nodulation in Vegetables. Plant Physiol 169:2761-2773. doi:10.1104/pp.15.01144.  
     

  • Wang G, Roux B, Feng F, Guy E, Li L, Li N, Zhang X, Lautier M, Jardinaud MF, Chabannes M, Arlat M, Chen S, He C, Noël LD, Zhou JM. 2015. The Decoy Substrate of a Pathogen Effector and a Pseudokinase Specify Pathogen-Induced Modified-Self Recognition and Immunity in Plants. Cell Host Microbe 18:285-295. doi: 10.1016/j.chom.2015.08.004.  
     

  • Alves-Carvalho S, Aubert G, Carrère S, Cruaud C, Brochot AL, Jacquin F, Klein A, Martin C, Boucherot K, Kreplak J, da Silva C, Moreau S, Gamas P, Wincker P, Gouzy J, Burstin J 2015. Full-length de novo assembly of RNA-seq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights into root nodulation in this species. Plant J 84:1-19. doi: 10.1111/tpj.12967.  
     

  • Venkateshwaran M, Jayaraman D, Chabaud M, Genre A, Balloon AJ, Maeda J, Forshey K, den Os D, Kwiecien NW, Coon JJ, Barker DG, Ané JM. 2015. A role for the mevalonate pathway in early plant symbiotic signaling. Proc Natl Acad Sci US A. 112:9781-9786. doi: 10.1073/pnas.1413762112.  
     

  • Clavijo F, Diedhiou I, Vaissayre V, Brottier L, Acolatse J, Moukouanga D, Crabos A, Auguy F, Franche C, Gherbi H, Champion A, Hocher V, Barker D, Bogusz D, Tisa LS, Svistoonoff S. 2015. The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytol 208:887-903. doi: 10.1111/nph.13506.  
     

  • Camps C, Jardinaud MF, Rengel D, Carrère S, Hervé C, Debellé F, Gamas P, Bensmihen S, Gough C. 2015. Combined genetic and transcriptomic analysis reveals three major signaling pathways activated by Myc-LCOs in Medicago truncatula. New Phytol208:224-240. doi: 10.1111/nph.13427.  
     

  • Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG. 2015. Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol 167:1233-1242. doi:10.1104/pp.114.253302.  
     

  • Laloum, T., Baudin, M., Frances, L., Lepage, A., Billault-Penneteau, B., Cerri, MR, Ariel, F., Jardinaud, MF., Gamas, P., de Carvalho-Niebel F,. and Niebel A. 2014. Two CCAAT box-binding transcription factors redundantly control early steps of legume-rhizobia endosymbiosis. Plant J 79:757-68. doi: 10.1111/tpj.12587.   
     

  • Formey, D., Sallet, E., Lelandais-Brière, C., Ben, C., Bustos-Sanmamed, P., Niebel, A., Frugier, F., Combier, J., Debellé, F., Hartmann , C., Poulain, J., Gavory, F., Wincker, P., Roux, C., Gentzbittel, L., Gouzy, J., Crespi, M. 2014. The small RNA diversity from Medicago truncatula roots under biotic interactions evidences the environmental plasticity of the miRNAome. Genome Biol. 15:457.  
     

  • Xiao, TT, Schilderink, S., Moling, S., Deinum, EE, Kondorosi, E., Franssen, H., Kulikova, O., Niebel, A., and Bisseling, T. 2014. Fate map of Medicago truncatula root nodes. Development 141:3517-28. doi: 10.1242/dev.110775.  
     

  • Rípodas, C., Clúa, J., Battaglia, M., Baudin, M., Niebel, A., Zanetti, ME, Blanco F. 2014. Transcriptional regulators of legume-rhizobia symbiosis: nuclear factors Ys and GRAS are two for tango. Plant Signal Behav. 9:e28847.  
     

  • Battaglia, M., Rípodas, C., Clúa, J., Baudin, M., Aguilar, OM, Niebel, A., Zanetti, ME, Blanco, FA 2014. A nuclear factor Y interacting protein of the GRAS family is required for nodule organogenesis, infection thread progression, and lateral root growth. Plant Physiol. 164(3):1430-42.   
     

  • Moreau, S., Fromentin, J., Vailleau, F., Vernié, T., Huguet, S., Balzergue, S., Frugier, F., Gamas, P., Jardinaud, MF. 2014. The symbiotic transcription factor MtEFD and cytokinins are positively acting in the Medicago truncatula and Ralstonia solanacearum pathogenic interaction. New Phytol 201,1343-1357.  
     

  • Roux, B., Rodde, N., Jardinaud, MF, 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., Gamas, P. 2014. An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser capture microdissection coupled to RNA-seq. Plant J 77, 817-837.  
     

  • Laporte, P., Lepage, A., Fournier, J., Catrice, O., Moreau, S., Jardinaud, MF., Mun, JH., Larrainzar, E., Cook, D., Gamas, P., Niebel, A. 2014. The CCAAT box-binding transcription factor MtNF-YA1 controls rhizobial infection. J Exp Bot 65, 481-494. 

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