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ENOD

ENDOSYMBIOTIC INFECTION AND NODULE DEVELOPMENT

Fernanda de Carvalho-Niebel
Andreas Niebel

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Nitrogen is a vital nutrient that supports plant growth, but it is often a limiting factor. Certain plant species overcome this limitation by establishing symbiotic relationships with nitrogen-fixing bacteria, which offer great potential to enhance the sustainability of agricultural systems. These interactions form specialized root organs, termed nodules, where bacteria are hosted intracellularly in an environment optimized for nitrogen metabolism. We study such nitrogen-fixing symbioses in legume plant species, interacting symbiotically with bacteria collectively called rhizobia. We seek to understand the cellular and molecular mechanisms underlying nodule development and rhizobial colonisation, as well as the genetic determinants that influence these symbioses in complex plant-plant interaction environments. We perform these studies using a range of legume and Brassicaceae species and various molecular, genetics, biochemistry and cell biology methodologies.

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RESEARCH THEMES

Main questions we would like to address are:

1. What are the molecular mechanisms behind symbiotic transcriptional reprogramming?

We focus on the study of main transcription factors and interconnected epigenetic reprograming that regulate nodule development in legumes. By combining functional genomics, transcription and chromatin biology-driven approaches in Medicago truncatula, we focus on understanding the mode of action of so-called pioneer transcription factors and chromatin regulators including long non-coding RNA (lncRNA) in symbiotic transcriptional reprogramming.

Contact: Matthias Benoit and Andreas Niebel.

 

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2. What are the cellular mechanisms orchestrating rhizobia infection of their legume host?

The transfer of rhizobia from the root surface to the nodule is a vital step directed by the plant, which is achieved via the establishment of a unique transcellular, tip-grown, apoplastic infection thread structure, or via intercellular spaces. However, underlying mechanisms remain poorly characterised. Here we combine functional genomics, biochemistry and high-resolution microscopy approaches in different model systems (e.g. M. truncatula, Aeschynomene evenia) to dissect cellular mechanisms behind these entry modes, with a particular focus on unravelling mechanisms behind the creation of cell polarity and a new cell wall interface to guide rhizobia root colonization.

Contact: Joëlle Fournier and Fernanda de Carvalho-Niebel.

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3. How do plant-plant interactions modulate rhizobia legume symbiosis ?

How plant-plant interactions may modulate key agricultural traits, such as nodulation in legumes, remains unknown. Here we combine high-throughput phenotyping, GWAS and functional genetics to elucidate genotype-dependent interactions that impact root nodulation in legumes.

Contact: Matthias Benoit.

Current projects

  • ANR PRC ADDORE (2025-2029), on “Cell polarity in root nodule symbioses”. Partners: S. Radutoiu (Aarhus, DK); D. Capela (LIPME). F. de Carvalho-Niebel (Coordinator).

  • ANR JCJC ISLAND (2025-2029), on “LncRNAs regulating gene expression during nodule development”. M. Benoit (Coordinator).

  • ANR PRC SYMBASE (2025-2029), on “How symbiotic infection is triggered in lateral root base”. JF Arrighi, PHIM (Coordinator), F. de Carvalho-Niebel (LIPME leader).

  • ANR PRC MELONOD (2024-2028), “Role of a pioneer transcription factor in the rhizobium symbiosis”. S. Jaubert & B. Favery (ISA, Nice). A. Niebel (Coordinator)

  • INRAE-SPE SYM2PLANTS (2024-2025), “Exploring the impact of plant-plant interactions on nitrogen-fixing root symbiosis in legumes". M. Benoit & M. Hanemian (Co-coordination).

  • IRP CNRS-LOCOSYM (2023-2027), “Long non-coding ARNs regulating rhizobia symbiosis". F. Ariel, F. Blanco & E. Zanetti (Argentina), Martin Crespi (France). A. Niebel (Coordinator).

MEMBERS

Thèmes de recherche
Membres

Former Members

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DANG Thi Thu (2021-2023)

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BENNION Anne (2022-2024)

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GUILLORY Ambre  (2021-2023)

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RUBIA GALIANO Maribel (2022; 2025)

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PUBLICATIONS

Publications and preprints 

 

Yang L, Frances L, de Carvalho-Niebel F, Frendo P, Boncompagni E. 2024. Identification of regulatory promoter sequences directing MtCP6 transcription at the onset of nodule senescence in Medicago truncatula. bioRxiv 2024.11.25.625165. doi: https://doi.org/10.1101/2024.11.25.625165 

 

Guillory, A., Fournier, J., Kelner, A. Hobecker K, Auriac MC, Frances L, Delers A, Pedinotti L, Le Ru A, Keller J, Delaux PM, Gutjahr C, Frei Dit Frey N, de Carvalho-Niebel F.  2024. Annexin- and calcium-regulated priming of legume root cells for endosymbiotic infection. Nat Commun 15, 10639. https://doi.org/10.1038/s41467-024-55067-3

de Carvalho-Niebel F, Fournier J, Becker A, Marín Arancibia M. 2024. Cellular insights into legume root infection by rhizobia. Curr Opin Plant Biol 81:102597.https://doi.org/10.1016/j.pbi.2024.102597

Kirolinko C, Hobecker K, Cueva M, Botto F, Christ A, Niebel A, Ariel F, Blanco FA, Crespi M, Zanetti ME. 2024. A lateral organ boundaries domain transcription factor acts downstream of the auxin response factor 2 to control nodulation and root architecture in Medicago truncatula. New Phytol 242:2746-2762. https://doi.org/10.1111/nph.19766

 

Zanetti ME, Blanco F, Ferrari M, Ariel F, Benoit M, Niebel A, Crespi M. 2024. Epigenetic control during root development and symbiosis. Plant Physiol Jun 12:kiae333. https://doi.org/10.1093/plphys/kiae333

 

Auriac MC, Griffiths C, Robin-Soriano A, Legendre A, Boniface MC, Muños S, Fournier J, Chabaud M. 2024. The penetration of sunflower root tissues by the parasitic plant Orobanche cumana is intracellular. New Phytol 241:2326-2332. https://doi.org/10.1111/nph.19495 

 

Jardinaud MF, Carrere S, Gourion B, Gamas P. 2023. Symbiotic Nodule Development and Efficiency in the Medicago truncatula Mtefd-1 Mutant is Highly Dependent on Sinorhizobium Strains. Plant Cell Physiol 64:27-42. https://doi.org/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. 8: 741–749  https://doi.org/10.1038/s41477-022-01188-w

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

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.  

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.

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 Commun 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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