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ENOD

ENDOSYMBIOTIC INFECTION AND NODULE DEVELOPMENT

Fernanda de Carvalho-Niebel
Andreas Niebel

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Endosymbiotic associations between plants and soil microorganisms play key roles in improving the supply of essential nutrients to the host plant.

We work on the nitrogen-fixing symbiotic interaction between legume plants and soil bacteria collectively known as rhizobia, which is of particular interest to reduce synthetic nitrogen fertilizer inputs in agriculture. This sophisticated interaction results in the development of a new root organ, called the root nodule, within which rhizobia are hosted to convert atmospheric nitrogen into forms the plant can use. The formation of this remarkable organ requires bacterial colonization and nodule development to occur in a tightly synchronized manner.

Our team uses the model legume Medicago truncatula to investigate the plant regulatory mechanisms that govern rhizobial infection, nodule development and their coordination. Our main scientific objectives are to understand (i) how the plant controls infection-related cell-type specific responses and (ii) how transcriptional and epigenetic regulatory mechanisms shape nodule development.

Our projects thus employ a range of approaches, from classical ones (molecular biology, genetics, transcriptomics, (epi)genomics and microscopy) to more advanced, cutting edge methods (in cell biology, reverse genetics and cell type-specific approaches) that we have recently adapted for Medicago.

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RESEARCH THEMES

Regulation and dynamics of rhizobial infection

Root colonization by rhizobia occurs in most species of Fabaceae legumes, via tubular structures, called infection threads, which guide the rhizobia transcellularly to the developing nodule primordium. The development of these structures by polar growth is essential to ensure the progressive colonization of the root cells and ultimately of the nodular primordium. Their construction is closely synchronized with the development of the nodule. In addition, the plant anticipates their initiation, thanks to the establishment of cellular reprogramming, preserved during evolution, and necessary to guide the entry of symbiotic microorganisms. Our main scientific objectives are to identify the key molecular players and cellular mechanisms underlying the development of the infection thread and associated cellular reprogramming.

 

We have identified transcriptional regulators that orchestrate the formation and progression of these infection structures in legumes (Andriankaja et al., 2007; Cerri et al., 2012, 2016, 2017; Liu et al., 2019a) and genetic pathways they regulate. We have also discovered cellular and intercellular mechanisms that regulate the formation or progression of infection threads in Medicago (Fournier et al., 2015; Kelner et al., 2018; Gaudioso-Pedraza et al., 2018; Liu et al. ., 2019b). We carry on these analyzes and also address the plant-bacteria cross-talk and the possible conservation of certain responses in a broader context of root symbioses.

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To answer these questions, we use complementary approaches in reverse genetics, transcriptomics (including cell-type specific), optical & electron microscopy and high resolution in vivo cell imaging in the model legume Medicago truncatula .

 

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Contact :

Fernanda de Carvalho-Niebel (DR2 CNRS), Joëlle Fournier (CRHC CNRS)

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Collaborations:

International: A. Becker (SYNMIKRO, Marburg, Germany); E. Larrainzar (University of Navarra, Pamplona, Spain); M. Marín (LMU, Munich, Germany); Peter Kaló (NAIK, Gödöllő, Hungary). National: F. Cartieaux, V. Hocher & S. Svistoonoff (LSTM, Montpellier); P. Frendo & E. Boncompagni (ISA, Sophia-Antipolis); Local: R. Peyraud (iMEAN, Toulouse); N. Frei-Dit-Frey, PM. Delaux & E. Jamet (LRSV, Toulouse).

Funding:

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ANR-DFG PRCI Live Switch (2020-2024), INRAE-SPE CREPE (2020-2023); FRAIB-AO-INTERUNITE-CROSS (2019-2022); ANR-DFG PRCI COME-IN (2015-2019).

Central regulators of nodular development

Nodule development in Medicago involves the mitotic activation of root cells following a precise pattern of cell divisions (Xiao et al., 2014). These divisions give rise to a new organ, called a nodule, composed of an apical meristem, allowing the growth of the nodule throughout its life, and successive zones of coordinated differentiation of bacterial and plant cells, to create the microenvironment suitable for symbiotic nitrogen fixation. In the team, we are studying regulators of these key phases of nodular development: (i) meristem formation and (ii) nodular differentiation.

The team identified NF-YA1, a transcription factor belonging to the  “CCAAT-box binding factors” family, as a key regulator of nodule development in Medicago (Combier et al., 2006; Laloum et al., 2013; Laloum et al., 2014; Laporte et al., 2014; Baudin et al., 2015). In addition to its contribution to early signaling and symbiotic infection, fate-map analysis revealed the crucial importance of NF-YA1 for the establishment of the nodular meristem (Xiao et al., 2014). In order to understand the mode of action of NF-YA1 in controlling this key process, we are currently identifying and characterizing the target genes of NF-YA1 (Shrestha et al., 2021). In addition, in animals, NF-Ys are considered to be pioneer transcription factors. As part of the PIOSYM ANR (2020-2024), the team is currently trying to demonstrate that NF-YA1 also has characteristics of a pioneer factor regulating the root-nodule transition.

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Thanks to the development of laser capture microdissection (LCM) -RNAseq approaches in Medicago, the team has generated valuable resources for the scientific community (Jardinaud et al., 2016; Roux et al., 2018), such as the first plant and rhizobium transcriptome of specific zones of the nodule (Roux et al., 2014; https://iant.toulouse.inra.fr/symbimics). This study and other previous work by the group have identified key plant regulators of nodular differentiation, including the ERF transcription factor EFD, which regulates cytokinin responses via RR4 (Vernié et al., 2008), and new epigenetic mechanisms.

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Indeed, the team demonstrated a precise spatial regulation of genes associated with DNA methylation in nodules, the key role of the DEMETER DNA demethylase for nodule differentiation and the preferential clustering of nodule differentiation genes. in genomic regions called symbiotic islands, enriched with epigenetic marks (Satgé et al., 2016; Pecrix et al., 2018).

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The group is currently continuing the analysis of these important transcriptional and epigenetic regulators of nodule differentiation.

Contact :

Andreas Niebel (DR2-CNRS), Pascal Gamas (DR1 CNRS)

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Collaborations:

International: F. Ariel (University of Santa Fe, Argentina); F. Blanco & E. Zanetti (University of La Plata, Argentina); E. Larrainzar (University of Navarra, Spain); K. Szczyglowski (University of Western Ontario, Canada); S. Sinharoy (National Institute of Plant Genome Research, New Delhi, India). National: M. Benhamed, M. Crespi, F. Frugier (IPS2, Paris-Saclay); P. Frendo (ISA, Sophia-Antipolis). Local: J. Gouzy (LIPME).

Funding:

ANR PIOSYM (2020-2024), CNRS-LIA (International Associated Laboratory) France-Argentina: NOCOSYM (2018-2021); ANR EPISYM (2016-2020); INRA-SPE (EFFOR, 2019-2020); INRAE-BAP (D-CRISPR, 2020-2021; coordination J. Gouzy); FRAIB MYCONODISLAND (2021-2022).

MEMBERS

Thèmes de recherche
Membres
Regulation
Régulateurs

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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