Publications

2024

  • Argirò, L., Laffont, C., Moreau, C., Moreau, C., Su, Y., Pervent, M., Parrinello, H., Blein, T., Kohlen, W., Lepetit, M., and Frugier, F. (2024). The Compact Root Architecture 2 systemic pathway is required for the repression of cytokinins and miR399 accumulation in Medicago truncatula N-limited plants. J. Exp. Bot., 75(18):5667-5680.

  • Gao, J.P., Su, Y., Jiang, S., Liang, W., Lou, Z., Frugier, F., Xu, P., and Murray, J.D. (2024). Applying conventional and cell-type-specific CRISPR/Cas9 genome editing in legume plants. aBIOTECH, s42994-024-00190-4.

  • Pedinotti, L., Teyssendier de la Serve, J., Roudaire, T., San Clemente, H., Aguilar, M., Kohlen, W., Frugier*, F., and Frei dit Frey*, N. (2024). The CEP peptide-CRA2 receptor module promotes arbuscular mycorrhizal symbiosis. Current Biol., S0960-9822(24)01326-5. (*, co-correponding authors)

 

2023

  • Fonouni-Farde, C., and Frugier, F. (2023). NODULE INCEPTION: a direct regulator of gibberellin biosynthesis during symbiotic nodulation. New Phytol., 239(2):449-451.

  • Ivanovici, A., Laffont, C., Larrainzar, E., Patel, N., Winning, C.S., Lee, H.G., Imin, N., Frugier, F., and Djordjevic, M.A. (2023). The Medicago SymCEP7 hormone increases nodule number via shoots without compromising lateral root number. Plant Physiol., 191(3):2012–2026.

  • Laffont, C., and Frugier, F. (2023). Rhizobium symbiotic efficiency meets CEP signaling peptides. New Phytol., 241(1):24-27.

  • Martin, ML.., Pervent, M., Lambert, I., Colella, S., Tancelin, M., Severac, D., Clément, G., Tillard, P., Frugier, F., and Lepetit, M. (2023). A localized osmotic stress activates systemic responses to N-limitation in Medicago truncatula-Sinorhizobium symbiotic plants. Frontiers Plant Sci., 14.



2022

  • Cervantes-Pérez, S.A., Thibivilliers, S., Laffont, C., Farmer, A.D., Frugier, F., and Libault M. (2022). Cell-specific pathways recruited for symbiotic nodulation in the Medicago truncatula legume. Mol Plant., 15(12):1868-1888.

  • Frugier, F. Editorial Feature: Meet the PCP Editor-Florian Frugier (2022). Plant Cell Physiol., 63(5):573–575.

  • Luo, Z., Moreau, C., Wang, J., Frugier, F., and Xie, F. (2022). NLP1 binds the CEP1 signaling peptide promoter to repress its expression in response to nitrate. New Phytol., 234:1547–1552.

  • Sauviac, L., Rémy, A., Huault, E., Dalmasso, M., Kazmierczak, T., Jardinaud, M.F., Legrand, L., Moreau, C., Ruiz, B., Cazalé, A.C., Valière, S., Gourion, B., Dupont, L., Gruber, V., Boncompagni, E., Meilhoc, E., Frendo, P., Frugier, F., and 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.

 

2021

  • Boyrie, L., Moreau, C., Frugier, F., Jacquet, C., and Bonhomme, M. (2021). A linkage disequilibrium-based statistical test for Genome-Wide Epistatic Selection Scans in structured populations. Heredity, 126(1):77-91.
  • Gautrat, P., Laffont, C., Frugier, F. and Ruffel, S. (2021). Nitrogen Systemic Signaling: From Symbiotic Nodulation to Root Acquisition. Trends Plant Sci., 26(4):392-406.
  • Moreau, C., Gautrat, P., and Frugier F. (2021). Nitrate-induced CLE35 signaling peptides inhibit nodulation through the SUNN receptor and miR2111 repression. Plant Physiol., 185(3):1216-1228. 

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2020

  • Chapman, K., Ivanovici, A., Taleski, M., Sturrock, C.J., Ng, J.L.P., Mohd-Radzman, N.A., Frugier, F., Bennett, M.J., Mathesius, U., and Djordjevic, M.A. (2020). CEP receptor signalling controls root system architecture in Arabidopsis and Medicago. New Phytol., 226(6):1809-1821.
  • Gautrat, P., Laffont, C., and Frugier, F. (2020). Compact Root Architecture 2 Promotes Root Competence for Nodulation through the miR2111 Systemic Effector. Curr Biol., 30(7):1339-1345. 

  • Kazmierczak, T., Yang,L., Boncompagni, E.,Meilhoc, E., Frugier, F., Frendo, P., Bruand, C., Gruber V., and Brouquisse, R. (2020). Legume nodule senescence: a coordinated death mechanism between bacteria and plant cells, Adv. Bot. Res., Chapter 7, pp.182-212. Elsevier Ed.
  • Laffont, C., Ivanovici, A., Gautrat, P., Brault, M., Djordjevic, M.A., and Frugier, F. (2020). The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically. Nat Commun., 11(1):3167.

  • Tan, S., Sanchez, M., Laffont, C., Boivin, S., Le Signor, C., Thompson, R.D., Frugier, F., and Brault, M. (2020). A cytokinin signalling type-B response regulator transcription factor acting in early nodulation. Plant Physiol., 183(3):1319-1330.
  • Zhu, F., Deng, J., Chen, H., Liu, P., Zheng, L., Ye, Q., Li, R., Brault, M., Wen, J., Frugier, F., Dong, J., and Wang, T. (2020). A CEP peptide receptor-like kinase regulates auxin biosynthesis and ethylene signaling to coordinate root growth and symbiotic nodulation in Medicago truncatula. Plant Cell, 32(9):2855-2877.

 

2019

  • Fonouni-Farde, C., Miassod, A., Laffont, C., Morin, H., Bendahmane, A., Diet, A., and Frugier F. (2019). Gibberellins negatively regulate the development of Medicago truncatula root system. Sci. Rep., 9(1):2335.
  • Gautrat, P., Mortier,V., Laffont, C., De Keyser, A., Fromentin, J., Frugier, F., and Goormachtig, S. (2019). Unraveling new molecular players involved in the autoregulation of nodulation in Medicago truncatula. J. Exp. Bot., 70(4):1407–1417.

  • Laffont, C., Huault, E., Gautrat, P., Endre, G., Kalo, P., Bourion, V., Duc, G., and Frugier F. (2019). Independent regulation of symbiotic nodulation by the SUNN negative and CRA2 positive systemic pathways. Plant Physiol., 180:559-570.

  • Tan, S., Debellé, F., Gamas, P., Frugier, F., and Brault, M. (2019). Diversification of cytokinin phosphotransfer signaling genes in Medicago truncatula and other legume genomes. BMC Genomics, 20(1):373.

 

2018

  • Fonouni-Farde, C., McAdam, E., Nichols, D., Diet, A., Foo, E., and Frugier, F. (2018). Cytokinins and the CRE1 receptor influence endogenous gibberellin levels in Medicago truncatula. Plant Signal. Behav., 26:e1428513.
  • Laffont, C., de Cuyper, C., Fromentin J., Mortier, V., de Keyser, A., Verplancke, C., Holsters, M., Goormachtig, S., and Frugier, F. (2018). MtNRLK1, a CLAVATA1-like leucine-rich repeat receptor-like kinase upregulated during nodulation in Medicago truncatula.  Sci. Rep., 8(1):2046.
  • Pecrix, Y., Staton, S.E., Sallet, E., Lelandais-Brière, C., Moreau, S., Carrère, S., Blein, T., Jardinaud, M.F., 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., and Gamas, P. (2018). Whole-genome landscape of Medicago truncatula symbiotic genes. Nat. Plants 4(12):1017-1025.s.

 

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2017

  •  Di Giacomo, E., Laffont, C., Sciarra, F., Iannelli, M.A., Frugier, F., and Frugis, G. (2017). KNAT3/4/5-like class 2 KNOX transcription factors are involved in Medicago truncatula symbiotic nodule organ development.   New Phytol., 213(2):822-837.
  • Fonouni-Farde, C., Kisiala, A., Brault,M., Emery, R.J.N., Diet, A., and Frugier, F. (2017). DELLA1-mediated gibberellin signaling regulates cytokinin-dependent symbiotic nodulation. Plant Phys., 175(4):1795-1806
  •  Ryu, H., Laffont, C., Frugier, F., and Hwang, I. (2017). MAP Kinase-Mediated Negative Regulation of Symbiotic Nodule Formation in Medicago truncatula.  Mol. Cells, 40, 17-23.

 

2016

  • Boivin, S., Kazmierczak, T., Brault, M., Wen, J., Gamas, P., Mysore, K.S., and Frugier, F. (2016). Different cytokinin CHK receptors regulate nodule initiation as well as later nodule developmental stages in Medicago truncatula.  Plant Cell Environ., 39:2198-209.
  • Boivin, S., Fonouni-Farde, C., and Frugier, F. (2016). How auxin and cytokinin phytohormones modulate root microbe interactions.  Front. Plant Sci., 7:1240.
  • Fonouni-Farde, C., Tan, S., Baudin, M., Brault, M., Wen, J., Mysore, K.M., Niebel, A., Frugier, F., and Diet, A. (2016). DELLA-mediated gibberellin signaling regulates Nod Factor signaling and rhizobial infection. Nat. Commun., 7:12636.
  • Jardinaud, M.F., Boivin, S., Rodde, N., Catrice, O., Kisiala, A., Lepage, A., Moreau, S., Roux, B., Cottret, L., Sallet, E., Brault, M., Emery, R.J., Gouzy, J., Frugier, F., and 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(3):2256-76.
  • Mohd-Radzman, N.A., Laffont, C., Ivanovici, A., Patel, N., Reid, D.E., Stougaard, J., Frugier, F., Imin, N., and Djordjevic, M.A. (2016). Different pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development. Plant Physiol., 171(4):2536-48.
  • Zhang, Z., Hu, X., Zhang, Y., Miao, Z., Xie, C., Meng, X., Deng, J., Wen, J., Mysore, K.S., Frugier, F., Wang, T., and Dong, J. (2016). Opposing control by transcription factors MYB61 and MYB3 increases freezing tolerance by relieving C-repeat Binding Factor suppression. Plant Physiol., 172:1306-23.

 

2015

  • Laffont, C., Rey, T., André, O., Novero, M., Kazmierczak, T., Debellé, F., Bonfante, P., Jacquet, C. and Frugier, F. (2015). The CRE1 cytokinin pathway is differentially recruited depending on Medicago truncatula root environments and negatively regulates resistance to a pathogen. Plos One 10(1):e0116819.
  • Ng, J.L., Hassan, S., Truong, T.T., Hocart, C.H., Laffont, C., Frugier, F., and Mathesius, U. (2015). Flavonoids and auxin transport inhibitors rescue symbiotic nodulation in the Medicago truncatula cytokinin perception mutant cre1. Plant Cell 27 (8):2210-26.

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2014

  • Bustos-Sanmamed, P., Hudik, E., Laffont, C., Reynes, C., Sallet, E., Wen, J., Mysore, K.S., Camproux, A.C., Hartmann, C., Gouzy, J., Frugier, F., Crespi, M. and Lelandais-Brière, C. (2014). A Medicago truncatula rdr6 allele impairs transgene silencing and endogenous phased siRNA production but not development. Plant Biotechnol. J. 12(9):1308-18.
  • Formey, D., Sallet, E., Lelandais-Brière, C., Ben, C., Bustos-Sanmamed, P., Niebel, A., Frugier, F., Combier, J.P., Debellé, F., Hartmann, C., Poulain, J., Gavory, F., Wincker, P., Roux, C., Gentzbittel, L., Gouzy, J. and 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.
  • Hopkins, J., Pierre, O., Kazmierczak, T., Gruber, V., Frugier, F., Clement, M., Frendo, P., Herouart, D., and Boncompagni, E. (2014). Mtzr1, A Praf protein, is involved in the development of roots and symbiotic root nodules in Medicago truncatula.  Plant Cell Environ. 37(3):658-69.
  • Huault, E., Laffont, C., Wen, J., Mysore, K.S., Ratet, P., Duc, G., and Frugier, F. (2014). Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase.  Plos Genet. 10(12):e1004891.
  • Moreau, S., Fromentin, J., Vailleau, F., Vernié, T., Huguet, S., Balzergue, S., Frugier, F., Gamas, P., and Jardinaud, M.F. (2014).The symbiotic transcription factor MtEFD and cytokinins are positively acting in the Medicago truncatula and Ralstonia solanacearum pathogenic interaction.  New Phytol. 201(4):1343-57.

 

2013

  • Bustos-Sanmamed, P., Laffont, C., Frugier, F., Lelandais-Brière, C., and Crespi M. (2013) Analyzing small and long RNAs in plant development using non-radiactive in situ hybridization. Methods Mol. Biol., Chapter 20, 959:303-16.
  • Bustos-Sanmamed, P., Laffont, C., Frugier, F., Lelandais-Brière, C., and Crespi M. (2013). Analyzing protein distribution in plant tissues using "whole-mount" immunolocalization. Methods Mol. Biol., Chapter 21, 959:317-22.
  • Heyl, A., Brault, M., Frugier, F., Kuderová, A., Lindner, A.C., Motyka, V., Rashotte, A.M., von Schwartzenberg, K., Vankova, R., and Schaller, E. (2013). Nomenclature for members of the two-component signaling pathway of plants.  Plant Physiol. 161(3):1063-5.
  • Nisa-Martínez, R., Laporte, P., Jiménez-Zurdo, J.I., Frugier, F., Crespi, M., and Toro N. (2013). Localization of a Bacterial Group II Intron-Encoded Protein in Eukaryotic Nuclear Splicing-Related Cell Compartments.  PLoS One 8(12):e84056.

 

2012

  • Ariel, F., Brault-Hernandez, M., Laffont, C., Huault, E., Brault, M., Plet, J., Moison, M., Blanchet, S., Ichanté, J.L., Chabaud, M., Carrere, S., Crespi, M., Chan, R.L., and Frugier, F. (2012). Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula.  Plant Cell 24(9):3838-52.
  • De Zélicourt, A., Diet, A., Marion, J., Laffont, C., Ariel, F., Moison, M., Zahaf, O., Crespi, M., Gruber, V., and Frugier, F. (2012). Dual involvement of a Medicago truncatula NAC transcription factor in root abiotic stress response and symbiotic nodule senescence.  Plant J. 70(2):220-30.
  • Laporte, P., Niebel, A., and Frugier, F. (2012). Legume roots and nitrogen-fixing symbiotic interactions. In : Root Genomics and Soil Interactions. Ed. M. Crespi, Chapter 9, 145-170. Wiley-Blackwell Publishing.
  • Zahaf, O., Blanchet, S., de Zélicourt, A., Alunni, B., Plet, J., Laffont, C., de Lorenzo, L., Imbeaud, S., Ichanté, J.L., Diet, A., Badri, M., Zabalza, A., González, E.M., Delacroix, H., Gruber, H., Frugier, F., and Crespi, M. (2012). Comparative transcriptomic analysis of salt adaptation in roots of contrasting Medicago truncatula genotypes.  Mol. Plant 5(5):1068-81.

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2011

  • D’haeseleer, K., Den Herder, G., Laffont, C., Plet, J., Mortier, V., Lelandais-Brière, C., De Bodt, S., De Keyser, A., Crespi, M., Holsters, M., Frugier, F., and Goormachtig, S. (2011). Transcriptional and posttranscriptional regulation of a NAC1 transcription factor in Medicago truncatula roots.  New Phytol. 191(3) : 647-61.
  • Morère-Le Paven, M.C., Viau, L., Hamon, A., Vandecasteele, C., Pellizzaro, A., Bourdin, C., Laffont, C., Lapied, B., Lepetit, M., Frugier, F., Legros, C., and Limami, A.M. (2011). Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula.  J. Exp. Bot. 62(15):5595-605.
  • Plet, J., Wasson, A., Ariel, F., Le Signor, C., Baker, D., Mathesius, U., Crespi, M., and Frugier, F. (2011). MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula.  Plant J. 65(4):622-33.

 

2010

  • Ariel, F. D., Diet, A., Crespi, M., and Chan R. (2010). The LOB-like transcription factor MtLBD1 controls Medicago truncatula root architecture under salt stress.  Plant Signal Behav. 5(12):1666-8.
  • Ariel, F., Diet, A., Verdenaud, M., Gruber, V., Frugier, F., Chan, R., and Crespi, M. (2010). Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1.  Plant Cell 22(7):2171-83.
  • Laffont, C., Blanchet, S., Lapierre, C., Brocard, L., Ratet, P., Crespi, M., Mathesius, U., and Frugier, F. (2010). The Compact Root Architecture 1 gene regulates lignification, flavonoid production and polar auxin transport in Medicago truncatula.  Plant Physiol. 153(4):1597-607.

 

2009

  • Gonzalez-Rizzo, S., Laporte, P., Crespi, M., and Frugier, F. (2009). Legume root architecture : a peculiar root system. In : Root development. Ed. T. Beeckman, Chapter 10, 239-287. Blackwell Publishing.

  • Gruber, V., Blanchet, S., Diet , A., Zahaf , O., Boualem, A., Kakar, K., Alunni, B., Udvardi, M., Frugier, F., and Crespi, M. (2009). Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula.  Mol. Genet. Genomics 281(1):55-66.
  • Lelandais-Brière, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., Gouzy, J., and Crespi, M. (2009). Genome-wide small RNA analysis revealed differentially regulated miRNA isoforms in Medicago truncatula roots and nodules.  Plant Cell 21(9):2780-96.
  • Merchan, F., Boualem, A., Crespi, M., and Frugier, F. (2009). Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins.  Genome Biol. 10(12):R136.

 

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2008

  • Boualem, A., Laporte, P., Jovanovic, M., Laffont, C., Plet, J., Combier, J.P., Niebel, A., Crespi, M., and Frugier, F. (2008). microRNA166 controls root and nodule development in Medicago truncatula.  Plant J. 54(5):876-87.
  • Chinchilla, D., Frugier, F., Raices, M., Merchan, F., Giammaria, V., Gargantini, P., Gonzalez-Rizzo, S., Crespi, M., and & Ulloa, R. (2008). A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots. Funct. Plant Biol. 35(1):92-101.
  • Crespi, M., and Frugier, F. (2008). De novo organ formation from a differentiated cells : root nodule organogenesis.  Sci. Signal. 1(49):re11.
  • Jovanovic, M., Lefebvre, V., Laporte, P., Gonzalez-Rizzo, S., Lelandais-Brière, C., Frugier, F., Hartmann, C., and Crespi, M. (2008). How the environment regulates root architecture in dicots. Adv. in Bot. Res. 46:35-74.
  • Vernié, T., Moreau, S., de Billy, F., Plet, J., Combier, J.P., Rogers, C., Oldroyd, G., Frugier, F., Niebel, A., and Gamas, P. (2008). EFD Is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula.  Plant Cell 20(10):2696-713.

 

2007

  • Hause, B., Frugier, F. and Crespi, M. (2007). Immunolocalization. In : Medicago truncatula Handbook (disponible sur http://www.noble.org/MedicagoHandbook/), Medicago truncatula protocol chapters : cytology and microscopy (ISBN 0-9754303-1-9).
  • De Lorenzo, L., Merchan, F., Blanchet, S., Megias, M., Frugier, F., Crespi, M., and Sousa, C. (2007). Differential expression of the TFIIIA regulatory pathway in response to salt stress between Medicago truncatula genotypes.  Plant Physiol. 145(4):1521-32.
  • Merchan, F., Crespi, M., and Frugier, F. (2007) .Response of Medicago truncatula to salt stress. In : Medicago truncatula Handbook (disponible sur http://www.noble.org/MedicagoHandbook/), Biology of Medicago truncatula (ISBN 0-9754303-1-9).

  • Merchan, F., de Lorenzo, L., Gonzalez Rizzo, S., Niebel, A., Manyani, H., Frugier, F., Sousa, C. and Crespi, M. (2007). Identification of regulatory pathways involved in the reacquisition of root growth after salt stress in Medicago truncatula.  Plant J. 51(1):1-17.

 

2006

  • Combier, J., Frugier, F., de Billy, F., Boualem, A., El-Yahyaoui, F., Moreau, S., Vernié, T., Ott, T., Gamas, P., Crespi, M., and Niebel, A. (2006). MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.  Genes & Dev. 20(22) : 3084-8. (commentaire dans "Molecular Biology Select”, Cell 127(7):1291-1293.)
  • Gargantini, P., Gonzalez-Rizzo, S., Chinchilla, D., Raices, M., Giammaria, V., Ulloa, R.F., Frugier, F. and Crespi, M. (2006). A CDPK isoform participates in the regulation of nodule number in Medicago truncatula.  Plant J. 48(6):843-56.
  • Gonzalez-Rizzo, S., Crespi, M. and Frugier, F. (2006). The M. truncatula Mt CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with S. meliloti.  Plant Cell 18(10):2680-93.    (commentaire dans “Plant Cell News in Brief” : 18(10):2419).

 

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