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1. Distinct genetic basis for root responses to lipo-chitooligosaccharide signal molecules from different microbial origins

Author

Guillaume Bécard, Christophe Jacquet, Olivier André, Virginie Puech-Pagès, Sylvain Cottaz, Emilie Amblard, Fabienne Maillet, Maxime Bonhomme, Magali Garcia, Sébastien Fort, Clare Gough, and Sandra Bensmihen

Subjects
Lipopolysaccharides, 0106 biological sciences, 0301 basic medicine, Root (linguistics), Kingdom Fungi, Physiology, Oligosaccharides, Chitin, Genome-wide association study, Plant Science, 01 natural sciences, Rhizobia, 03 medical and health sciences, Mycorrhizae, Medicago truncatula, Symbiosis, Legume, Genetics, Chitosan, biology, fungi, Heritability, biology.organism_classification, Phenotype, 030104 developmental biology, Genome-Wide Association Study, Signal Transduction, 010606 plant biology & botany
Abstract

Lipo-chitooligosaccharides (LCOs) were originally found as symbiotic signals called Nod Factors (Nod-LCOs) controlling the nodulation of legumes by rhizobia. More recently, LCOs were also found in symbiotic fungi and, more surprisingly, very widely in the kingdom Fungi, including in saprophytic and pathogenic fungi. The LCO-V(C18:1, fucosylated/methyl fucosylated), hereafter called Fung-LCOs, are the LCO structures most commonly found in fungi. This raises the question of how legume plants such as Medicago truncatula can discriminate between Nod-LCOs and Fung-LCOs. To address this question, we performed a genome-wide association study on 173 natural accessions of M. truncatula, using a root branching phenotype and a newly developed local score approach. Both Nod-LCOs and Fung-LCOs stimulated root branching in most accessions, but the root responses to these two types of LCO molecules were not correlated. In addition, the heritability of the root response was higher for Nod-LCOs than for Fung-LCOs. We identified 123 loci for Nod-LCO and 71 for Fung-LCO responses, of which only one was common. This suggests that Nod-LCOs and Fung-LCOs both control root branching but use different molecular mechanisms. The tighter genetic constraint of the root response to Fung-LCOs possibly reflects the ancestral origin of the biological activity of these molecules.

Published
2021
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2. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Author

Candice L. Swift, Arthur QuyManh Maes, Nancy P. Keller, Cristobal Carrera Carriel, Kevin Garcia, Guillaume Bécard, Joanna Tannous, Quanita J. Choudhury, Jean-Michel Ané, Michelle A. O’Malley, Junko Maeda, Jin Woo Bok, Michelle Keller-Pearson, Tomás Allen Rush, Patricia Jargeat, Virginie Puech-Pagès, Sylvain Cottaz, Michael R. Sussman, Fabienne Maillet, Jeniel E. Nett, Adeline Bascaules, Jessy Labbé, Kevin R. Cope, Alexandra Haouy, Bailey Kleven, Véréna Poinsot, Chad J. Johnson, Sébastien Fort, Corinne Lefort, Devanshi Khokhani, Fort, Sébastien, University of Wisconsin-Madison, Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, Evolution des Interactions Plantes-Microorganismes, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Interactions moléculaires et réactivité chimique et photochimique (IMRCP), Institut de Chimie de Toulouse (ICT-FR 2599), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), South Dakota State University (SDSTATE), North Carolina State University [Raleigh] (NC State), University of North Carolina System (UNC), The University of Tennessee [Knoxville], University of Georgia [USA], University of California [Santa Barbara] (UC Santa Barbara), University of California (UC), Centre de Recherches sur les Macromolécules Végétales (CERMAV), Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA), Université Fédérale Toulouse Midi-Pyrénées, Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, University of California [Santa Barbara] (UCSB), University of California, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Fluides, Energie, Réacteurs, Matériaux et Transferts (FERMAT), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), BIBAC - Chimie analytique et interactions biomolécules - matière molle biomimétique (BIBAC), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT), and ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017)

Subjects
0301 basic medicine, Hypha, Science, General Physics and Astronomy, Oligosaccharides, Chitin, 02 engineering and technology, Biology, General Biochemistry, Genetics and Molecular Biology, Article, Microbiology, Microbial ecology, 03 medical and health sciences, Fungal biology, Pseudohyphal growth, Symbiosis, Ascomycota, Mycorrhizae, Spore germination, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Cellular microbiology, Fungal ecology, lcsh:Science, [SDV.BBM.BC] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Chitosan, Multidisciplinary, Ecology, Phylum, Basidiomycota, Fatty Acids, fungi, Fungi, General Chemistry, Spores, Fungal, 021001 nanoscience & nanotechnology, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Spore, 030104 developmental biology, lcsh:Q, 0210 nano-technology, Bacteria, Rhizobium, Signal Transduction
Abstract

Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development., Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by certain bacteria and fungi that establish symbiotic relationships with plants. Here, the authors show that LCOs are produced also by many other, non-symbiotic fungi, and regulate fungal growth and development.

Published
2020
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3. Distinct genetic bases for plant root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins

Author

Magali Garcia, Christophe Jacquet, Maxime Bonhomme, Sébastien Fort, Guillaume Bécard, Emilie Amblard, Fabienne Maillet, Sandra Bensmihen, Virginie Puech-Pagès, Sylvain Cottaz, Clare Gough, Olivier André, Centre de Recherches sur les Macromolécules Végétales (CERMAV), Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA), Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées, Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Chimie du CNRS (INC)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS), ANR-14-CE18-0008,NICE CROPS,Bio-stimulateurs chitiniques naturels pour une agriculture durable(2014), ANR-11-INBS-0010,METABOHUB,Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation(2011), ANR-11-LABX-0003,ARCANE,Grenoble, une chimie bio-motivée(2011), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), ANR-15-IDEX-0002,UGA,IDEX UGA(2015), ANR-16-CRNT-0005,Innovation Chimie Carnot,Innovation Chimie Carnot(2016), and ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010)

Subjects
0106 biological sciences, [SDV]Life Sciences [q-bio], Genome-wide association study, Nod, 01 natural sciences, lateral root development, Rhizobia, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, 03 medical and health sciences, lipo-chitooligosaccharides, Medicago truncatula, GWAS, [CHIM]Chemical Sciences, Legume, 030304 developmental biology, Genetics, 0303 health sciences, biology, fungi, Plant root, food and beverages, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, Heritability, biology.organism_classification, Phenotype, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Nod Factors, 010606 plant biology & botany
Abstract

SummaryLipo-chitooligosaccharides (LCOs) were originally found as symbiotic signals called Nod Factors (Nod-LCOs) controlling nodulation of legumes by rhizobia. More recently LCOs were also found in symbiotic fungi and, more surprisingly, very widely in the kingdom fungi including in saprophytic and pathogenic fungi. The LCO-V(C18:1, Fuc/MeFuc), hereafter called Fung-LCOs, are the LCO structures most commonly found in fungi. This raises the question of how legume plants, such asMedicago truncatula, can perceive and discriminate between Nod-LCOs and these Fung-LCOs.To address this question, we performed a Genome Wide Association Study on 173 natural accessions ofMedicago truncatula, using a root branching phenotype and a newly developed local score approach.Both Nod- and Fung-LCOs stimulated root branching in most accessions but there was very little correlation in the ability to respond to these types of LCO molecules. Moreover, heritability of root response was higher for Nod-LCOs than for Fung-LCOs. We identified 123 loci for Nod-LCO and 71 for Fung-LCO responses, but only one was common.This suggests that Nod- and Fung-LCOs both control root branching but use different molecular mechanisms. The tighter genetic constraint of the root response to Fung-LCOs possibly reflects the ancestral origin of the biological activity of these molecules.

Published
2020
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4. Sinorhizobium meliloti succinylated high molecular weight succinoglycan and the Medicago truncatula LysM receptor‐like kinase MtLYK10 participate independently in symbiotic infection

Author

Fabienne Maillet, Hajeewaka C. Mendis, Pascal Ratet, Clare Gough, Kathryn M. Jones, Kirankumar S. Mysore, Jiangqi Wen, Million Tadege, Joëlle Fournier, Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Plant Biology Division, The Samuel Roberts Noble Foundation, Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)), Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Basic Research Program, SAIC-Frederick, National Science Foundation (NSF) :DBI-0703285, IOS-1127155, European Commission, United States Department of Agriculture (USDA) : 2014-67013-21579, CNRS, ANR-15-CE20-0004,AOI,Autoregulation de l'infection dans la symbiose rhizobium-legumineuses(2015), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), and Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)

Subjects
0106 biological sciences, 0301 basic medicine, symbiotic nitrogen fixation, [SDV]Life Sciences [q-bio], Mutant, Lotus japonicus, microbiome, Plant Science, infection thread, Root hair, beneficial microbes, exopolysaccharide, LysM-receptor-like kinase, Medicago truncatula, root hair, Sinorhizobium meliloti, succinoglycan, 01 natural sciences, 03 medical and health sciences, Symbiosis, Nitrogen Fixation, Genetics, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, ComputingMilieux_MISCELLANEOUS, Plant Proteins, Medicago, Vegetal Biology, biology, Phosphotransferases, Polysaccharides, Bacterial, fungi, food and beverages, Cell Biology, biology.organism_classification, Cell biology, Molecular Weight, 030104 developmental biology, Phenotype, Mutation, bacteria, Root Nodules, Plant, Bacteria, Biologie végétale, 010606 plant biology & botany
Abstract

International audience; The formation of nitrogen-fixing nodules on legume hosts is a finely tuned process involving many components of both symbiotic partners. Production of the exopolysaccharide succinoglycan by the nitrogen-fixing bacterium Sinorhizobium meliloti 1021 is needed for an effective symbiosis with Medicago spp., and the succinyl modification to this polysaccharide is critical. However, it is not known when succinoglycan intervenes in the symbiotic process, and it is not known whether the plant lysin-motif receptor-like kinase MtLYK10 intervenes in recognition of succinoglycan, as might be inferred from work on the Lotus japonicus MtLYK10 ortholog, LjEPR3. We studied the symbiotic infection phenotypes of S. meliloti mutants deficient in succinoglycan production or producing modified succinoglycan, in wild-type Medicago truncatula plants and in Mtlyk10 mutant plants. On wild-type plants, S. meliloti strains producing no succinoglycan or only unsuccinylated succinoglycan still induced nodule primordia and epidermal infections, but further progression of the symbiotic process was blocked. These S. meliloti mutants induced a more severe infection phenotype on Mtlyk10 mutant plants. Nodulation by succinoglycan-defective strains was achieved by in trans rescue with a Nod factor-deficient S. meliloti mutant. While the Nod factor-deficient strain was always more abundant inside nodules, the succinoglycan-deficient strain was more efficient than the strain producing only unsuccinylated succinoglycan. Together, these data show that succinylated succinoglycan is essential for infection thread formation in M. truncatula, and that MtLYK10 plays an important, but different role in this symbiotic process. These data also suggest that succinoglycan is more important than Nod factors for bacterial survival inside nodules.

Published
2020
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5. Endosymbiotic Sinorhizobium meliloti modulate Medicago root susceptibility to secondary infection via ethylene

Author

Fabienne Maillet, Chrystel Gibelin-Viala, Jacques Batut, David Rengel, Catherine Masson-Boivin, Clare Gough, Fernando Sorroche, Christian Chervin, Anne-Marie Garnerone, Lan Zou, Mathilda Walch, Véréna Poinsot, Centre National de la Recherche Scientifique - CNRS (FRANCE), Institut National Polytechnique de Toulouse - Toulouse INP (FRANCE), Institut National de la Recherche Agronomique - INRA (FRANCE), Université Toulouse III - Paul Sabatier - UT3 (FRANCE), Laboratoire des interactions plantes micro-organismes (LIPM), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), Interactions moléculaires et réactivité chimique et photochimique (IMRCP), Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie de Toulouse (ICT-FR 2599), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées, Génomique et Biotechnologie des Fruits (GBF), Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Supérieure Agronomique de Toulouse-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes, Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Fluides, Energie, Réacteurs, Matériaux et Transferts (FERMAT), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-École nationale supérieure agronomique de Toulouse (ENSAT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Université de Toulouse (UT), ANR ‘Nice Crops’ project (ANR‐14‐CE18‐0008‐02), ANR AOI (ANR‐15‐CE20‐0004‐01), China Scholarship Council, ‘Laboratoire d'Excellence (LABEX)’ TULIP (ANR‐10‐LABX‐41)., European Project: 267196,EC:FP7:PEOPLE,FP7-PEOPLE-2010-COFUND,AGREENSKILLS(2012), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-École nationale supérieure agronomique de Toulouse [ENSAT]-Institut National Polytechnique (Toulouse) (Toulouse INP), Institut National Polytechnique de Toulouse - INPT (FRANCE), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Institut National Polytechnique (Toulouse) (Toulouse INP), and Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)

Subjects
0106 biological sciences, 0301 basic medicine, Agronomie, Physiology, Secondary infection, [SDV]Life Sciences [q-bio], Mutant, [SDV.SA.AGRO]Life Sciences [q-bio]/Agricultural sciences/Agronomy, Plant Science, Root hair, Models, Biological, Plant Root Nodulation, Plant Roots, 01 natural sciences, Plant Epidermis, Rhizobia, Microbiology, 03 medical and health sciences, Ethylene, Bacterial Proteins, Symbiosis, Medicago truncatula, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, ComputingMilieux_MISCELLANEOUS, Plant Diseases, [SDV.EE]Life Sciences [q-bio]/Ecology, environment, Volatile Organic Compounds, Sinorhizobium meliloti, Medicago, biology, Légume, food and beverages, Ethylenes, biology.organism_classification, [SDV.BV.PEP]Life Sciences [q-bio]/Vegetal Biology/Phytopathology and phytopharmacy, 030104 developmental biology, Rhizobium, Infection, 010606 plant biology & botany
Abstract

International audience; A complex network of pathways coordinates nodulation and epidermal root hair infection in the symbiotic interaction between rhizobia and legume plants. Whereas nodule formation was known to be autoregulated, it was so far unclear whether a similar control is exerted on the infection process. We assessed the capacity of Medicago plants nodulated by Sinorhizobium meliloti to modulate root susceptibility to secondary bacterial infection or to purified Nod factors in split-root and volatile assays using bacterial and plant mutant combinations. Ethylene implication in this process emerged from gas production measurements, use of a chemical inhibitor of ethylene biosynthesis and of a Medicago mutant affected in ethylene signal transduction. We identified a feedback mechanism that we named AOI (for Autoregulation Of Infection) by which endosymbiotic bacteria control secondary infection thread formation by their rhizospheric peers. AOI involves activation of a cyclic adenosine 30,50-monophosphate (cAMP) cascade in endosymbiotic bacteria, which decreases both root infectiveness and root susceptibility to bacterial Nod factors. These latter two effects are mediated by ethylene. AOI is a novel component of the complex regulatory network controlling the interaction between Sinorhizobium meliloti and its host plants that emphasizes the implication of endosymbiotic bacteria in fine-tuning the interaction.

Published
2019
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6. The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots

Author

Nathaniel Schleif, Steven H. Strauss, Emmeline Fung, Sara S. Jawdy, Heike Bücking, Jessy Labbé, Edward Steigerwald, Fabienne Maillet, Tomás Allen Rush, Virginie Puech-Pagès, Kimberly G. Schnell, Kevin R. Cope, Muthusubramanian Venkateshwaran, Junko Maeda, Jean-Michel Ané, Cathleen Ma, Kevin Garcia, Guillaume Bécard, Jonathan Setzke, Patricia Jargeat, Yunqian Wang, Adeline Bascaules, Thomas B. Irving, University of Wisconsin-Madison, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Oregon State University (OSU), Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, South Dakota State University (SDSTATE), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Evolution des Interactions Plantes-Microorganismes, Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), United States Department of Agriculture (USDA) : 2017-67014-26530 WIS01695, National Science Foundation (NSF) : DGE-1256259, United States Department of Energy (DOE) : DE-SC0018247, National Science Foundation (NSF) : 1546742, 1331098, Tree Genomics and Biosafety Cooperative at Oregon State University, NSF Center for Advanced Forestry Systems : 1238305, Plant-Microbe Interfaces Scientific Focus Area in the Genomic Science Program, Office of Biological and Environmental Research in the DOE, Office of Science, United States Department of Energy (DOE) : DE-AC05-00OR22725, ANR-14-CE18-0008,NICE CROPS,Bio-stimulateurs chitiniques naturels pour une agriculture durable(2014), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), ANR-11-INBS-0010,METABOHUB,Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation(2011), Erist, Montpellier, Appel à projets générique - Bio-stimulateurs chitiniques naturels pour une agriculture durable - - NICE CROPS2014 - ANR-14-CE18-0008 - Appel à projets générique - VALID, Towards a Unified theory of biotic Interactions: the roLe of environmental - - TULIP2010 - ANR-10-LABX-0041 - LABX - VALID, Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation - - METABOHUB2011 - ANR-11-INBS-0010 - INBS - VALID, Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), and Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
0106 biological sciences, 0301 basic medicine, Lipopolysaccharides, MESH: Signal Transduction, [SDV]Life Sciences [q-bio], Plant Science, Fungus, Biology, Root hair, Photosynthesis, MESH: Plant Roots / microbiology, 01 natural sciences, MESH: Lipopolysaccharides / chemistry, [SDV.BV.BOT] Life Sciences [q-bio]/Vegetal Biology/Botanics, Laccaria, 03 medical and health sciences, Symbiosis, Laccaria bicolor, MESH: Calcium / metabolism, Mycorrhizae, Botany, MESH: Populus / metabolism, Colonization, MESH: Gene Expression Regulation, Plant, MESH: Mycorrhizae / physiology, Research Articles, [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Lateral root, fungi, Cell Biology, [SDV.EE.IEO] Life Sciences [q-bio]/Ecology, environment/Symbiosis, 15. Life on land, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, MESH: Laccaria / metabolism, 030104 developmental biology, Populus, MESH: Symbiosis / physiology, Actinorhizal plant, 010606 plant biology & botany, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wildtype Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.

Published
2019
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7. Lipo‐chitooligosaccharides promote lateral root formation and modify auxin homeostasis in Brachypodium distachyon

Author

Fabienne Maillet, Benoit Lefebvre, Luis Buendia, Devin O'Connor, Sandra Bensmihen, Quitterie van de-Kerkhove, Saïda Danoun, Clare Gough, Laboratoire des interactions plantes micro-organismes (LIPM), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), Sainsbury Laboratory Cambridge, University of Cambridge [UK] (CAM), Laboratoire de Recherche en Sciences Végétales (LRSV), Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Sainsbury Laboratory Cambridge University (SLCU), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), INRA/SPE project 'LCAux', French 'Ministere de l'Enseignement Superieur et de la Recherche', ANR-11-IDEX-0002,UNITI,Université Fédérale de Toulouse(2011), and ANR-16-CE20-0025,WHEATSYM,ROLES DES SIGNAUX MICROBIENS LCO/CO ET DE LEURS RECEPTEURS DE PLANTES DANS DES INTERACTIONS BENEFIQUES ENTRE MONOCOTYLEDONES ET MICROORGANISMES DU SOL(2016)

Subjects
0106 biological sciences, 0301 basic medicine, Indoles, hormone homeostasis, Physiology, Oligosaccharides, lateral root primordia, Chitin, Endogeny, Plant Science, root architecture, indole-3-butyric acid (IBA), Models, Biological, Plant Roots, 01 natural sciences, Fluorescence, 03 medical and health sciences, lipochitooligosaccharide (LCO), Auxin, Nod factors, Homeostasis, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, heterocyclic compounds, Gene, Lateral root formation, ComputingMilieux_MISCELLANEOUS, chemistry.chemical_classification, Chitosan, Indoleacetic Acids, biology, Auxin homeostasis, Chemistry, fungi, food and beverages, biology.organism_classification, Lipids, Medicago truncatula, Cell biology, auxin dosage, 030104 developmental biology, Brachypodium, Brachypodium distachyon, symbiotic signal, Signal Transduction, 010606 plant biology & botany
Abstract

International audience; . Lipo-chitooligosaccharides (LCOs) are microbial symbiotic signals that also influence root growth. In Medicago truncatula, LCOs stimulate lateral root formation (LRF) synergistically with auxin. However, the molecular mechanisms of this phenomenon and whether it is restricted to legume plants are not known. . We have addressed the capacity of the model monocot Brachypodium distachyon (Brachypodium) to respond to LCOs and auxin for LRF. For this, we used a combination of root phenotyping assays, live-imaging and auxin quantification, and analysed the regulation of auxin homeostasis genes. We show that LCOs and a low dose of the auxin precursor indole-3-butyric acid (IBA) stimulated LRF in Brachypodium, while a combination of LCOs and IBA led to different regulations. Both LCO and IBA treatments locally increased endogenous indole-3-acetic acid (IAA) content, whereas the combination of LCO and IBA locally increased the endogenous concentration of a conjugated form of IAA (IAA-Ala). LCOs, IBA and the combination differentially controlled expression of auxin homeostasis genes. . These results demonstrate that LCOs are active on Brachypodium roots and stimulate LRF probably through regulation of auxin homeostasis. The interaction between LCO and auxin treatments observed in Brachypodium on root architecture opens interesting avenues regarding their possible combined effects during the arbuscular mycorrhizal symbiosis.

Published
2018
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8. Adapting the Lateral Root-Inducible System to Medicago truncatula

Author

Violaine Herrbach, Fabienne Maillet, Sandra Bensmihen, Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)

Subjects
0106 biological sciences, 0301 basic medicine, chemistry.chemical_classification, biology, Host (biology), fungi, Lateral root, food and beverages, biology.organism_classification, 01 natural sciences, Medicago truncatula, Rhizobia, Transcriptome, 03 medical and health sciences, 030104 developmental biology, chemistry, Auxin, Arabidopsis, Botany, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Legume, ComputingMilieux_MISCELLANEOUS, 010606 plant biology & botany
Abstract

Almost all legume plants have the capacity to form two types of root organs: lateral roots and nodules (that will host rhizobia that fix nitrogen). Transcriptomic analyses are useful to understand both the similarities and differences between nodule and LR formation and to compare the LR developmental programs used by Arabidopsis and model legumes such as Medicago truncatula. However, in M. truncatula as in Arabidopsis, root cells "committed" to LR formation programs are scattered along the primary root and localized in the inner most layers of the root. To gain access to these cells, a lateral root-inducible system (LRIS) was first developed in Arabidopsis. This LRIS was recently shown to be effective in maize as well. Here we present a LRIS protocol adapted to the model legume Medicago truncatula. Using the same auxin transporter inhibitor and permeant auxin molecules used for Arabidopsis and maize but with slight modifications in their concentrations, we obtained very efficient enrichment and synchronization in LR development stages in M. truncatula.

Published
2018
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9. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza

Author

Fabienne Maillet, Hugues Driguez, Véréna Poinsot, Guillaume Bécard, Andreas Niebel, Laurence Cromer, Damien Formey, Jean Dénarié, Olivier André, Virginie Puech-Pagès, Eduardo Andres Martinez, Delphine Giraudet, Monique Gueunier, Alexandra Haouy, inconnu, Inconnu, Centre de Recherches sur les Macromolécules Végétales (CERMAV), Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Joseph Fourier - Grenoble 1 (UJF), Unité mixte de recherche interactions plantes-microorganismes, Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées, Evolution des Interactions Plantes-Microorganismes, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Recherches sur les Macromolécules Végétales, Centre National de la Recherche Scientifique (CNRS), EMD Crop BioScience, Charles-Leopold Mayer Prize, French Academy of Sciences, Institut National de la Recherche Agronomique, Carret, Michèle, Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), and Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT)

Subjects
Lipopolysaccharides, EXTRACTS CHEMISTRY METABOLISM, 0106 biological sciences, ved/biology.organism_classification_rank.species, Plant Roots, 01 natural sciences, CHOMATOGRAPHY HIGH PRESSURE LIQUID, LIPOPOLYSACCHARIDES CHEMISTRY METABOLISM, Glomeromycota, Mycorrhizae, Mycorrhiza, Chromatography, High Pressure Liquid, ComputingMilieux_MISCELLANEOUS, 0303 health sciences, Multidisciplinary, Endosymbiosis, Ecology, SIGNAL TRANSDUCTION, SYMBIOSIS, food and beverages, SPORES FUNGAL CHEMISTRY METABOLISM SYMBIOSIS, Spores, Fungal, GLOMEROMYCOTA METABOLISM, MEDICAGO TRUNCATULA CHEMISTRY GROWTH & DEVELOPMENT METABOLISM MICROBIOLOBY, Medicago truncatula, Daucus carota, Arbuscular mycorrhiza, MYCORRHIZAE METABOLISM, PLANT ROOTS CHEMISTRY GROWTH & DEVELOPMENT METABOLISM MICROBIOLOGY, CARBOHYDRATE SEQUENCE, CAROTA CHEMISTRY METABOLISM MICROBIOLOGY, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, Biology, 03 medical and health sciences, Symbiosis, Terrestrial plant, Botany, MOLECULAR SEQUENCE DATA, PLANT, 030304 developmental biology, Plant Extracts, ved/biology, fungi, Fabaceae, 15. Life on land, biology.organism_classification, DAUCUS, AM, SUSTAINABLE DEVELOPMENT, 010606 plant biology & botany
Abstract

International audience; Arbuscular mycorrhiza (AM) is a root endosymbiosis between plants and glomeromycete fungi. It is the most widespread terrestrial plant symbiosis, improving plant uptake of water and mineral nutrients. Yet, despite its crucial role in land ecosystems, molecular mechanisms leading to its formation are just beginning to be unravelled. Recent evidence suggests that AM fungi produce diffusible symbiotic signals. Here we show that Glomus intraradices secretes symbiotic signals that are a mixture of sulphated and non-sulphated simple lipochitooligosaccharides (LCOs), which stimulate formation of AM in plant species of diverse families (Fabaceae, Asteraceae and Umbelliferae). In the legume Medicago truncatula these signals stimulate root growth and branching by the symbiotic DMI signalling pathway. These findings provide a better understanding of the evolution of signalling mechanisms involved in plant root endosymbioses and will greatly facilitate their molecular dissection. They also open the way to using these natural and very active molecules in agriculture.

Published
2011
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10. Activation of Symbiosis Signaling by Arbuscular Mycorrhizal Fungi in Legumes and Rice

Author

Enrico Gobbato, Eric Samain, Jean-Michel Ané, Fabienne Maillet, Richard J. Morris, Muthusubramanian Venkateshwaran, Jongho Sun, Emma Granqvist, Sylvain Cottaz, Giles E. D. Oldroyd, Sébastien Fort, Audrey Wiley-Kalil, Jean Dénarié, J. Benjamin Miller, Cell and Developmental Biology, John Innes Centre [Norwich], Biologie et Génétique des Interactions Plante-Parasite (UMR BGPI), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Centre de Recherches sur les Macromolécules Végétales (CERMAV), Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Joseph Fourier - Grenoble 1 (UJF), Department of Primary Care and Population Health [London] (PCPH), University College of London [London] (UCL), Department of Bacteriology, Veterinary Laboratories Agency, European Research Council as 'SYMBIOSIS,' the Bill and Melinda Gates Foundation, the Biotechnology and Biological Sciences Research Council as BB/J004553/1, Labex Arcane, ICMG as FR2607, and the Gatsby Charitable Foundation as a Sainsbury PhD fellowship, Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), and Université Joseph Fourier - Grenoble 1 (UJF)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)

Subjects
Lipopolysaccharides, 0106 biological sciences, [SDV]Life Sciences [q-bio], Molecular Sequence Data, Lotus japonicus, Oligosaccharides, chemistry.chemical_element, Chitin, Plant Science, Fungus, Calcium, 01 natural sciences, 03 medical and health sciences, Symbiosis, Gene Expression Regulation, Plant, Mycorrhizae, Medicago truncatula, Botany, Calcium Signaling, Research Articles, ComputingMilieux_MISCELLANEOUS, Glucuronidase, 030304 developmental biology, Chitosan, 0303 health sciences, Oryza sativa, biology, Lateral root, fungi, food and beverages, Oryza, Cell Biology, biology.organism_classification, chemistry, Seedlings, Lotus, Bacteria, Signal Transduction, 010606 plant biology & botany
Abstract

Establishment of arbuscular mycorrhizal interactions involves plant recognition of diffusible signals from the fungus, including lipochitooligosaccharides (LCOs) and chitooligosaccharides (COs). Nitrogen-fixing rhizobial bacteria that associate with leguminous plants also signal to their hosts via LCOs, the so-called Nod factors. Here, we have assessed the induction of symbiotic signaling by the arbuscular mycorrhizal (Myc) fungal-produced LCOs and COs in legumes and rice (Oryza sativa). We show that Myc-LCOs and tetra-acetyl chitotetraose (CO4) activate the common symbiosis signaling pathway, with resultant calcium oscillations in root epidermal cells of Medicago truncatula and Lotus japonicus. The nature of the calcium oscillations is similar for LCOs produced by rhizobial bacteria and by mycorrhizal fungi; however, Myc-LCOs activate distinct gene expression. Calcium oscillations were activated in rice atrichoblasts by CO4, but not the Myc-LCOs, whereas a mix of CO4 and Myc-LCOs activated calcium oscillations in rice trichoblasts. In contrast, stimulation of lateral root emergence occurred following treatment with Myc-LCOs, but not CO4, in M. truncatula, whereas both Myc-LCOs and CO4 were active in rice. Our work indicates that legumes and non-legumes differ in their perception of Myc-LCO and CO signals, suggesting that different plant species respond to different components in the mix of signals produced by arbuscular mycorrhizal fungi.

Published
2015
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11. The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling

Author

Clare Gough, R. Catoira, Christine Galera, Douglas R. Cook, Fabienne Maillet, Antonius C.J. Timmers, R.V. Penmetsa, and Jean Dénarié

Subjects
Lipopolysaccharides, Mutant, Root hair, Genes, Plant, Microtubules, Plant Roots, Rhizobia, Nod factor, Bacterial Proteins, Acetyltransferases, Microtubule, Botany, Symbiosis, Molecular Biology, Plant Proteins, Sinorhizobium meliloti, integumentary system, biology, fungi, Cell Polarity, Membrane Proteins, food and beverages, biology.organism_classification, Medicago truncatula, Cell biology, Phenotype, Mutation, Rhizobium, Medicago sativa, Developmental Biology
Abstract

The symbiotic infection of the model legume Medicago truncatula by Sinorhizobium meliloti involves marked root hair curling, a stage where entrapment of the microsymbiont occurs in a chamber from which infection thread formation is initiated within the root hair. We have genetically dissected these early symbiotic interactions using both plant and rhizobial mutants and have identified a M. truncatula gene, HCL, which controls root hair curling. S. meliloti Nod factors, which are required for the infection process, induced wild-type epidermal nodulin gene expression and root hair deformation in hcl mutants, while Nod factor induction of cortical cell division foci was reduced compared to wild-type plants. Studies of the position of nuclei and of the microtubule cytoskeleton network of hcl mutants revealed that root hair, as well as cortical cells, were activated in response to S. meliloti. However, the asymmetric microtubule network that is typical of curled root hairs, did not form in the mutants, and activated cortical cells did not become polarised and did not exhibit the microtubular cytoplasmic bridges characteristic of the pre-infection threads induced by rhizobia in M. truncatula. These data suggest that hcl mutations alter the formation of signalling centres that normally provide positional information for the reorganisation of the microtubular cytoskeleton in epidermal and cortical cells.

Published
2001
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12. Rhizobial lipochitooligosaccharide nodulation factors activate expression of the legume early nodulin gene ENOD12 in rice

Author

Swapan K. Datta, Fabienne Maillet, Pallavolu M. Reddy, Jagdish K. Ladha, Karabi Datta, Marilou C. Ramos, Norman Oliva, Rowena J. Hernandez, and Lina Torrizo

Subjects
Oryza sativa, Rhizobiaceae, biology, fungi, food and beverages, Cell Biology, Plant Science, Nod, biology.organism_classification, Genetically modified rice, Cell biology, Rhizobia, Nod factor, Pericycle, Botany, Genetics, Rhizobium
Abstract

Summary Lipochitooligosaccharide nodulation factors (Nod factors) produced by rhizobia are a major host range determinant. These factors play a pivotal role in the molecular signal exchange, infection and induction of symbiotic developmental responses in legumes leading to the formation of a nodule in which rhizobia carry out N2 fixation. Determining whether rice (Oryza sativa) can respond to Nod factors could lead to strategies that would make rice amenable to develop a nitrogen-fixing endosymbiotic association with rhizobia. We introduced into rice the promoter of the infection-related geneMtENOD12 (fromMedicago truncatula) fused to the β-glucuronidase (GUS) reporter gene to serve as a molecular marker to aid in the detection of Nod factor signal perception by rice cells. Treatment of the transgenic rice roots with Nod factors (10–6–10–9m) under nitrogen-limiting conditions induced MtENOD12-GUS expression in cortical parenchyma, endodermis and pericycle. In contrast, chitooligosaccharide backbone alone failed to elicit such a response in the root tissues. These findings demonstrate that rice roots perceive Nod factors and that these lipochitooligosaccharides, but not simple chitin oligomers, act as signal molecules in activatingMtENOD12 in cortical parenchyma as in legumes. Exogenous application ofN-naphthaleneacetic acid mimicked the Nod factor-elicited tissue-specific expression ofMtENOD12 in roots while cytokinins inhibited it, thus evidencing that Nod factors, auxin and cytokinins probably act on similar signaling elements responsible for the regulation ofMtENOD12 activation in rice. Taken together, these results suggest that at least a portion of the signal transduction machinery important for legume nodulation is likely to exist in rice.

Published
1998
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13. Transcriptional Responses toward Diffusible Signals from Symbiotic Microbes Reveal MtNFP- and MtDMI3-Dependent Reprogramming of Host Gene Expression by Arbuscular Mycorrhizal Fungal Lipochitooligosaccharides

Author

Claudia Hogekamp, Lisa F. Czaja, Natalija Hohnjec, Helge Küster, Patrick Lamm, Jean Dénarié, Fabienne Maillet, Eduardo Andres Martinez, Eric Samain, Leibniz University Hannover, Unité mixte de recherche interactions plantes-microorganismes, Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université Joseph Fourier - Grenoble 1 (UJF), Deutsche Forschungsgemeinschaft [SPP1212, KU-1478/4-1, KU-1478/4-2, KU-1478/4-3], inconnu, Inconnu, Centre de Recherches sur les Macromolécules Végétales (CERMAV), and Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Joseph Fourier - Grenoble 1 (UJF)

Subjects
0106 biological sciences, Physiology, [SDV]Life Sciences [q-bio], Mutant, Plant Science, CA2+ SPIKING, 01 natural sciences, Nod factor, MEDICAGO-TRUNCATULA ROOTS, 03 medical and health sciences, Botany, Gene expression, INFECTION, Genetics, LOTUS-JAPONICUS, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, CORTICAL-CELLS, Transcription factor, EARLY NODULIN, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, Regulation of gene expression, 0303 health sciences, Sinorhizobium meliloti, biology, RECEPTOR, PREPENETRATION APPARATUS, biology.organism_classification, Medicago truncatula, Cell biology, TRANSDUCTION PATHWAY, Signal transduction, LEGUME, 010606 plant biology & botany
Abstract

The formation of root nodules and arbuscular mycorrhizal (AM) roots is controlled by a common signaling pathway including the calcium/calmodulin-dependent kinase Doesn’t Make Infection3 (DMI3). While nodule initiation by lipochitooligosaccharide (LCO) Nod factors is well characterized, diffusible AM fungal signals were only recently identified as sulfated and nonsulfated LCOs. Irrespective of different outcomes, the perception of symbiotic LCOs in Medicago truncatula is mediated by the LysM receptor kinase M. truncatula Nod factor perception (MtNFP). To shed light on transcriptional responses toward symbiotic LCOs and their dependence on MtNFP and Ca2+ signaling, we performed genome-wide expression studies of wild-type, Nod-factor-perception mutant1, and dmi3 mutant roots challenged with Myc- and Nod-LCOs. We show that Myc-LCOs lead to transient, quick responses in the wild type, whereas Nod-LCOs require prolonged incubation for maximal expression activation. While Nod-LCOs are most efficient for an induction of persistent transcriptional changes, sulfated Myc-LCOs are less active, and nonsulfated Myc-LCOs display the lowest capacity to activate and sustain expression. Although all symbiotic LCOs up-regulated a common set of genes, discrete subsets were induced by individual LCOs, suggesting common and specific functions for these in presymbiotic signaling. Surprisingly, even sulfated fungal Myc-LCOs and Sinorhizobium meliloti Nod-LCOs, having very similar structures, each elicited discrete subsets of genes, while a mixture of both Myc-LCOs activated responses deviating from those induced by single treatments. Focusing on the precontact phase, we identified signaling-related and transcription factor genes specifically up-regulated by Myc-LCOs. Comparative gene expression studies in symbiotic mutants demonstrated that transcriptional reprogramming by AM fungal LCOs strictly depends on MtNFP and largely requires MtDMI3.

Published
2012
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14. Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2- O -Methylfucosylated Lipochitooligosaccharides for nod Gene–Dependent Interaction with Aeschynomene Plants

Author

Fabienne Maillet, Eric Giraud, Adeline Renier, Véréna Poinsot, Nico Nouwen, Joël Fardoux, Laboratoire des symbioses tropicales et méditerranéennes (UMR LSTM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université Montpellier 1 (UM1)-Institut de Recherche pour le Développement (IRD)-Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Interactions moléculaires et réactivité chimique et photochimique (IMRCP), Institut de Chimie de Toulouse (ICT), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Fluides, Energie, Réacteurs, Matériaux et Transferts (FERMAT), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), This work was supported by grants from the French national research agency (ANR-NEWNOD-2006-BLAN-0095 and ANR-SESAM-2010-BLAN-170801)., Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Institut de Chimie de Toulouse (ICT-FR 2599), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées, and NOUWEN, NICO

Subjects
Lipopolysaccharides, biochemistry and molecular biology, Root nodule, Physiology, [SDV]Life Sciences [q-bio], plant sciences, Nod, Plant Roots, milieu aquatique, nitrogen, Nod factor, Genes, Reporter, Bradyrhizobium, Photosynthesis, ComputingMilieux_MISCELLANEOUS, [SDV.EE]Life Sciences [q-bio]/Ecology, environment, 0303 health sciences, Plant Stems, biology, Strain (chemistry), food and beverages, Fabaceae, General Medicine, bacterium, photosynthetic, roots, biotechnology and applied microbiology, Flavanones, Nitrogen fixation, Root Nodules, Plant, symbiose, Signal Transduction, Molecular Sequence Data, Amidohydrolases, Microbiology, 03 medical and health sciences, Bacterial Proteins, Symbiosis, Nitrogen Fixation, Nitrogenase, Botany, Fucose, 030304 developmental biology, Flavonoids, 030306 microbiology, Aeschynomene, Gene Expression Regulation, Bacterial, biology.organism_classification, Genes, Bacterial, légume tropical, Agronomy and Crop Science, Bradyrhizobium japonicum
Abstract

Bradyrhizobium sp. strain ORS285 is a photosynthetic bacterium that forms nitrogen-fixing nodules on the roots and stems of tropical aquatic legumes of the Aeschynomene genus. The symbiotic interaction of Bradyrhizobium sp. strain ORS285 with certain Aeschynomene spp. depends on the presence of nodulation (nod) genes whereas the interaction with other species is nod gene independent. To study the nod gene-dependent molecular dialogue between Bradyrhizobium sp. strain ORS285 and Aeschynomene spp., we used a nodB-lacZ reporter strain to monitor the nod gene expression with various flavonoids. The flavanones liquiritigenin and naringenin were found to be the strongest inducers of nod gene expression. Chemical analysis of the culture supernatant of cells grown in the presence of naringenin showed that the major Nod factor produced by Bradyrhizobium sp. strain ORS285 is a modified chitin pentasaccharide molecule with a terminal N-C18:1-glucosamine and with a 2-O-methyl fucose linked to C-6 of the reducing glucosamine. In this respect, the Bradyrhizobium sp. strain ORS285 Nod factor is the same as the major Nod factor produced by the nonphotosynthetic Bradyrhizobium japonicum USDA110 that nodulates the roots of soybean. This suggests a classic nod gene-dependent molecular dialogue between Bradyrhizobium sp. strain ORS285 and certain Aeschynomene spp. This is supported by the fact that B. japonicum USDA110 is able to form N2-fixing nodules on both the roots and stems of Aeschynomene afraspera.

Published
2011
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15. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation

Author

R. Varma Penmetsa, Douglas R. Cook, Clare Gough, Giles E. D. Oldroyd, Besma Ben Amor, Sharon R. Long, Fabienne Maillet, Sidney L. Shaw, and Jean Dénarié

Subjects
Lipopolysaccharides, Mutant, Wasp Venoms, Plant Science, Nod, Root hair, Genes, Plant, Plant Roots, Chromosomes, Plant, Nod factor, Gene Expression Regulation, Plant, Calcium flux, Genetics, Medicago, Calcium Signaling, Regulation of gene expression, biology, Genetic Complementation Test, Cell Biology, biology.organism_classification, Physical Chromosome Mapping, Plants, Genetically Modified, Medicago truncatula, Phenotype, Mutation, Intercellular Signaling Peptides and Proteins, Calcium, Signal transduction, Peptides, Rhizobium, Signal Transduction
Abstract

Establishment of the Rhizobium-legume symbiosis depends on a molecular dialogue, in which rhizobial nodulation (Nod) factors act as symbiotic signals, playing a key role in the control of specificity of infection and nodule formation. Using nodulation-defective (Nod-) mutants of Medicago truncatula to study the mechanisms controlling Nod factor perception and signalling, we have previously identified five genes that control components of a Nod factor-activated signal transduction pathway. Characterisation of a new M. truncatula Nod- mutant led to the identification of the Nod Factor Perception (NFP) locus. The nfp mutant has a novel phenotype among Nod- mutants of M. truncatula, as it does not respond to Nod factors by any of the responses tested. The nfp mutant thus shows no rapid calcium flux, the earliest detectable Nod factor response of wild-type plants, and no root hair deformation. The nfp mutant is also deficient in Nod factor-induced calcium spiking and early nodulin gene expression. While certain genes controlling Nod factor signal transduction also control the establishment of an arbuscular mycorrhizal symbiosis, the nfp mutant shows a wild-type mycorrhizal phenotype. These data indicate that the NFP locus controls an early step of Nod factor signal transduction, upstream of previously identified genes and specific to nodulation.

Published
2003

16. Nodule-Inducing Activity of Synthetic Sinorhizobium meliloti Nodulation Factors and Related Lipo-Chitooligosaccharides on Alfalfa. Importance of the Acyl Chain Structure1

Author

Denis Tailler, G. Truchet, Kyriacos C. Nicolaou, Fabienne Maillet, Jean-Claude Promé, Nathalie Demont-Caulet, Jean-Claude Jacquinet, Jean-Marie Beau, and Jean Dénarié

Subjects
Lipopolysaccharides, Rhizobiaceae, Physiology, Molecular Sequence Data, Plant Science, Acylation, chemistry.chemical_compound, Structure-Activity Relationship, Sulfation, Chitin, Tetramer, Genetics, Symbiosis, Sinorhizobium meliloti, biology, food and beverages, biology.organism_classification, chemistry, Biochemistry, Carbohydrate Sequence, Plant protein, lipids (amino acids, peptides, and proteins), Bacteria, Research Article, Medicago sativa
Abstract

Sinorhizobium meliloti nodulation factors (NFs) elicit a number of symbiotic responses in alfalfa (Medicago sativa) roots. Using a semiquantitative nodulation assay, we have shown that chemically synthesized NFs trigger nodule formation in the same range of concentrations (down to 10−10m) as natural NFs. The absence of O-sulfate orO-acetate substitutions resulted in a decrease in morphogenic activity of more than 100-fold and approximately 10-fold, respectively. To address the question of the influence of the structure of the N-acyl chain, we synthesized a series of sulfated tetrameric lipo-chitooligosaccharides (LCOs) having fatty acids of different lengths and with unsaturations either conjugated to the carbonyl group (2E) or located in the middle of the chain (9Z). A nonacylated, sulfated chitin tetramer was unable to elicit nodule formation. Acylation with short (C8) chains rendered the LCO active at 10−7m. The optimal chain length was C16, with the C16-LCO being more than 10-fold more active than the C12- and C18-LCOs. Unsaturations were important, and the diunsaturated 2E,9Z LCO was more active than the monounsaturated LCOs. We discuss different hypotheses for the role of the acyl chain in NF perception.

Published
1999

17. Rhizobium Nod Factor Structure and the Phylogeny of Temperate Legumes

Author

Odile Schiltz, M. Ferro, Jean-Claude Promé, Jean Dénarié, C. Vialas, Arlette Savagnac, Guo-Ping Yang, Frédéric Debellé, and Fabienne Maillet

Subjects
Genetics, Sinorhizobium meliloti, biology, fungi, food and beverages, Nod, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, Bradyrhizobium, Rhizobia, Nod factor, Sinorhizobium, Azorhizobium, Botany, bacteria, Rhizobium
Abstract

The family Leguminosae is one of the largest families of flowering plants, including more than 18,000 species (Young, Johnston, 1989). Their symbiotic bacterial partners are very diverse and do not form a discrete clade. Although they are collectively referred to as rhizobia, they are now classified in distinct Rhizobium, Bradyrhizobium, Azorhizobium and Sinorhizobium (Young, Haukka, 1996). Some rhizobia are indeed more closely related to nonsymbiotic bacteria than they are to other rhizobia. However, all rhizobial species possess common nodulation (nod) genes, the nodABC genes, and consequently produce nodulation signals, the Nod factors, that belong to the same chemical family: they are chitin oligomers of 4 or 5 glucosamine residues that are mono-N-acylated at the terminal non-reducing end. The common chitin oligomer core can be substituted at both ends of the molecule, and each rhizobial species or biovar produces a set of major Nod factors with characteristic substitutions (Denarie et al., 1996). These substitutions are under the control of specific nod genes. In the case of Sinorhizobium meliloti, it has been shown that the three substitutions are essential for effective infection of the host plant, alfalfa. The structure of major Nod factors has now been determined for most rhizobial species and their comparison indicates that Nod factor structure is related to rhizobial host range (Denarie et al., 1996).

Published
1998
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18. The common nodABC genes of Rhizobium meliloti are host-range determinants

Author

Georges Truchet, Jean Dénarié, Myriam Ferro, Jean-Claude Promé, Claire Plazanet, Fabienne Maillet, Philippe Roche, and Frédéric Debellé

Subjects
Genotype, Acylation, Mutant, Molecular Sequence Data, Biology, N-Acetylglucosaminyltransferases, Polymerase Chain Reaction, Amidohydrolases, 03 medical and health sciences, chemistry.chemical_compound, Plasmid, Suppression, Genetic, Chitin, Symbiosis, Bacterial Proteins, Gene, 030304 developmental biology, 0303 health sciences, Multidisciplinary, 030306 microbiology, food and beverages, biochemical phenomena, metabolism, and nutrition, Biological Sciences, biology.organism_classification, Aminosugar, Biochemistry, chemistry, Carbohydrate Sequence, Rhizobium, Acyltransferases, Symbiotic bacteria, Medicago sativa, Plasmids, Sinorhizobium meliloti
Abstract

Symbiotic bacteria of the genus Rhizobium synthesize lipo-chitooligosaccharides, called Nod factors (NFs), which act as morphogenic signal molecules on legume hosts. The common nodABC genes, present in all Rhizobium species, are required for the synthesis of the core structure of NFs. NodC is an N -acetylglucosaminyltransferase, and NodB is a chitooligosaccharide deacetylase; NodA is involved in N-acylation of the aminosugar backbone. Specific nod genes are involved in diverse NF substitutions that confer plant specificity. We transferred to R. tropici , a broad host-range tropical symbiont, the ability to nodulate alfalfa, by introducing nod genes of R. meliloti . In addition to the specific nodL and nodFE genes, the common nodABC genes of R. meliloti were required for infection and nodulation of alfalfa. Purified NFs of the R. tropici hybrid strain, which contained chitin tetramers and were partly N-acylated with unsaturated C16 fatty acids, were able to elicit nodule formation on alfalfa. Inactivation of the R. meliloti nodABC genes suppressed the ability of the NFs to nodulate alfalfa. Studies of NFs from nodA , nodB , nodC , and nodI mutants indicate that ( i ) NodA of R. meliloti , in contrast to NodA of R. tropici , is able to transfer unsaturated C16 fatty acids onto the chitin backbone and ( ii ) NodC of R. meliloti specifies the synthesis of chitin tetramers. These results show that allelic variation of the common nodABC genes is a genetic mechanism that plays an important role in signaling variation and in the control of host range.

Published
1996

19. The Genetics of Rhizobium Host Range Control: Allelic and Non-Allelic Variation

Author

Georges Truchet, Claire Plazanet, Jean Dénarié, Frédéric Debellé, Fabienne Maillet, N. Demont, Charles Rosenberg, Maryvonne Ardourel, Philippe Roche, C. Pujol, Jean-Claude Promé, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), INRA - Laboratoire de biologie moleculaire des relations plantes microorganismes, Toulouse, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and ProdInra, Migration

Subjects
Genetics, 0303 health sciences, Medicago, biology, Host (biology), [SDV]Life Sciences [q-bio], food and beverages, biology.organism_classification, Pisum, [SDV] Life Sciences [q-bio], 03 medical and health sciences, Vicia, 0302 clinical medicine, Rhizobium, Melilotus, Phaseolus, Gene, 030217 neurology & neurosurgery, 030304 developmental biology
Abstract

The symbiotic association between Rhizobium and legumes is specific. For example R. meliloti nodulates Medicago, Melilotus and Trigonella species, R. tropici nodulates Phaseolus and Leucaena, and R. leguminosarum bv viciae ’s hosts belong to the Vicia and Pisum genera (van Rhijn, Vanderleyden, 1995). The bacterial genes controlling nodulation and host specificity (nod, nol and noe genes) have been classified into 3 groups: (i) The regulatory nodD genes activate the expression of the other nodulation genes in response to compounds secreted by the host plants. (ii) The common nodABC genes are found in all rhizobial species studied so far and are considered as functionally conserved between these species, (iii) The species-specific nod genes, such as nodH, nodL or nodFE in R. meliloti, determine the host range. Mutations in the latter genes generally result in an alteration of the host spectrum. In addition, these genes are required for transferring the host range between different rhizobial species

Published
1995
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20. In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species

Author

Georges Truchet, Philippe Roche, Jean-Claude Promé, Fabienne Maillet, Charles Rosenberg, Gilles Lortet, Maryvonne Ardourel, ProdInra, Migration, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA)

Subjects
Lipopolysaccharides, Operon, Molecular Sequence Data, Mutant, Regulatory Sequences, Nucleic Acid, Biology, Plant Roots, Regulon, Microbiology, Open Reading Frames, 03 medical and health sciences, Bacterial Proteins, Species Specificity, Acetyltransferases, Amino Acid Sequence, Symbiosis, Molecular Biology, Gene, [SDV.MP] Life Sciences [q-bio]/Microbiology and Parasitology, 030304 developmental biology, Genetics, 0303 health sciences, Medicago, 030306 microbiology, Chromosome Mapping, food and beverages, Acetylation, Sequence Analysis, DNA, biology.organism_classification, Medicago truncatula, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Carbohydrate Sequence, Medicago littoralis, Genes, Bacterial, Regulatory sequence, Rhizobium, Medicago sativa, Sinorhizobium meliloti
Abstract

In Rhizobium meliloti, the genes required for nodulation of legume hosts are under the control of DNA regulatory sequences called nod boxes. In this paper, we have characterized three host-specific nodulation genes, which form a flavonoid-inducible operon down-stream of the nod box n5. The first gene of this operon is identical to the nodL gene identified by Baev and Kondorosi (1992) in R. meliloti strain AK631. The product of the second gene, NoeA, presents some homology with a methyltransferase. nodL mutants synthesize Nod factors lacking the O-acetate substituent. In contrast, in strains carrying a mutation in either noeA or noeB, no modification in Nod-factor structure or production could be detected. On particular hosts, such as Medicago littoralis, mutants of the n5 operon showed a very weak nodule-forming ability, associated with a drastic decrease in the number of infection threads, while nodulation of Medicago truncatula or Melilotus alba was not affected. Thus, nodL noeA and noeB are host-specific nodulation genes. By using a gain-of-function approach, we showed that the presence of nodL, and hence of O-acetylated Nod factors, is a major prerequisite for confering the ability to nodulate alfalfa upon the heterologous bacterium Rhizobium tropici.

Published
1995

21. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-1)-hydroxylated fatty acids

Author

Jean-Claude Promé, M. Ferro, Jean Dénarié, N. Demont, Danielle Promé, Fabienne Maillet, and Maryvonne Ardourel

Subjects
Operon, Acylation, Molecular Sequence Data, Restriction Mapping, Oligosaccharides, Nod, Hydroxylation, General Biochemistry, Genetics and Molecular Biology, Mass Spectrometry, Microbiology, Rhizobia, Sulfation, Bacterial Proteins, Transcription (biology), Nitrogen Fixation, Genes, Regulator, Cloning, Molecular, Molecular Biology, Gene, Regulator gene, General Immunology and Microbiology, biology, General Neuroscience, Fatty Acids, food and beverages, biology.organism_classification, DNA-Binding Proteins, Lipid A, Biochemistry, Carbohydrate Sequence, Genes, Bacterial, Trans-Activators, Rhizobium, Research Article, Medicago sativa, Sinorhizobium meliloti, Transcription Factors
Abstract

Rhizobia elicit the formation of nitrogen-fixing nodules on specific legume hosts. Rhizobium meliloti nodulation (nod) genes control a signal exchange between the two symbiotic partners during infection and the early steps of nodulation. The regulatory nodD1, nodD2 and nodD3 genes are involved in the specific perception of different plant and environmental signals and activate the transcription of the nod operons. Once activated, the structural nod genes specify the synthesis of diffusible lipo-oligosaccharides, the Nod factors, which signal back to the plant. R. meliloti Nod factors are sulfated chito-oligosaccharides which are mono-N-acylated by unsaturated C16 fatty acids or by a series of C18 to C26 (omega-1)-hydroxylated fatty acids. In this paper we show that the regulatory nodD3 gene and another symbiotic regulatory gene, syrM, which mediate bacterial responses to plant signals that differ from those involving nodD1 and nodD2, determine the synthesis of Nod factors with different acyl moieties. nodD3 and syrM are required for the synthesis of Nod factors N-acylated by the (omega-1)-hydroxylated fatty acids. This regulatory mechanism makes possible the qualitative adaptation of bacterial Nod signal production to plant signals in the course of the symbiotic process.

Published
1994

22. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses

Author

Fabienne Maillet, Jean-Claude Promé, Jean Dénarié, F. de Billy, N. Demont, Georges Truchet, Maryvonne Ardourel, Frédéric Debellé, ProdInra, Migration, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, and Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)

Subjects
0106 biological sciences, Lipopolysaccharides, Mutant, Molecular Sequence Data, Oligosaccharides, Receptors, Cell Surface, Plant Science, Cell Communication, Root hair, 01 natural sciences, Models, Biological, Plant Roots, Mass Spectrometry, Microbiology, Nod factor, Cell wall, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, 03 medical and health sciences, Species Specificity, [SDV.GEN.GPL] Life Sciences [q-bio]/Genetics/Plants genetics, Tip growth, Symbiosis, Gene, 030304 developmental biology, 0303 health sciences, biology, 030306 microbiology, INDUCTION, ENOD40, food and beverages, Cell Biology, biology.organism_classification, Carbohydrate Sequence, Genes, Bacterial, Mutation, Rhizobium, Biological Assay, 010606 plant biology & botany, Research Article, Medicago sativa, Sinorhizobium meliloti
Abstract

Rhizobium meliloti produces lipochitooligosaccharide nodulation NodRm factors that are required for nodulation of legume hosts. NodRm factors are O-acetylated and N-acylated by specific C16-unsaturated fatty acids. nodL mutants produce non-O-acetylated factors, and nodFE mutants produce factors with modified acyl substituents. Both mutants exhibited a significantly reduced capacity to elicit infection thread (IT) formation in alfalfa. However, once initiated, ITs developed and allowed the formation of nitrogen-fixing nodules. In contrast, double nodF/nodL mutants were unable to penetrate into legume hosts and to form ITs. Nevertheless, these mutants induced widespread cell wall tip growth in trichoblasts and other epidermal cells and were also able to elicit cortical cell activation at a distance. NodRm factor structural requirements are thus clearly more stringent for bacterial entry than for the elicitation of developmental plant responses.

Published
1994

23. Rhizobium Nodulation Factors: Variations on a Theme

Author

Jean-Claude Promé, Georges Truchet, Charles Rosenberg, Fabienne Maillet, Jean Dénarié, Franck Talmont, Frédéric Debellé, Danielle Promé, N. Demont, Maryvonne Ardourel, Philippe Roche, William J. Broughton, Biserka Relic, N. P. J. Price, and Hélène Aurelle

Subjects
chemistry.chemical_compound, biology, Chitin, chemistry, Biochemistry, Glucosamine, Acetylation, Rhizobium, Nod, biology.organism_classification, Gene, Homology (biology), Rhizobia
Abstract

Nodulation (nod) genes of Rhizobium, which control infection, nodulation and host specificity, determine the production of extracellular lipo-oligosaccharidic Nod factors. The Nod factors of various rhizobia, including the narrow host-range temperate R. meliloti and the broad host-range tropical Rhizobium sp. NGR234 belong to the same chemical family: they are mono-N-acylated and substituted chitin oligomers. The common nodC gene codes for a protein which has homology with chitin synthases and may be involved in the synthesis of the chitin backbone. The species-specific nod genes determine the decoration of these core molecules by encoding substitutions with specific groups at particular sites. For example in R. meliloti (i) the nodH and nodPQ genes are involved in the O-sulfation of the lipooligosaccharides on the carbon 6 of the reducing glucosamine; (ii) the nodL gene is required for the O-acetylation of the carbon 6 of the non-reducing terminal glucosamine; (iii) the nodFE genes specify the synthesis of the specific C16:2 N-acyl chain. Rhizobium sp. NGR234 secretes a large family of Nod factors carrying a variety of substituents. The non-reducing end is N-acylated with vaccenic or palmitic acids, is N-methylated, and carries varying numbers of carbamoyl groups. The reducing glucosamine residue is substituted on position 6 with 2-O-methyl-L-fucose which may be acetylated, or sulfated, or non-substituted. The O-acetylation and the O-sulfation are mutually exclusive: thus this broad host range strain secretes a variety of charged and uncharged Nod factors. We also present data which strongly suggest that the host range nod genes mediate host specificity by determining the type of substitutions decorating the lipo-oligosaccharidic Nod factors.

Published
1993
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24. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated

Author

N. P. J. Price, Franck Talmont, Danielle Promé, Astrid Lewin, Steven G. Pueppke, Jean-Claude Promé, Jean Dénarié, Fabienne Maillet, William J. Broughton, Biserka Relic, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and ProdInra, Migration

Subjects
Lipopolysaccharides, Rhizobiaceae, [SDV]Life Sciences [q-bio], Molecular Sequence Data, Restriction Mapping, Microbiology, Mass Spectrometry, Vigna, chemistry.chemical_compound, Glucosamine, Cloning, Molecular, Phaseoleae, Symbiosis, Molecular Biology, Chromatography, High Pressure Liquid, Medicago, biology, Molecular Structure, Macroptilium, Sulfates, food and beverages, Acetylation, BIOLOGIE MOLECULAIRE, biology.organism_classification, [SDV] Life Sciences [q-bio], Vicia, ddc:580, chemistry, Biochemistry, Carbohydrate Sequence, Genes, Bacterial, Rhizobium, Plasmids
Abstract

Rhizobium species strain NGR234 is the most promiscuous known rhizobium. In addition to the non-legume Parasponia andersonii, it nodulates at least 70 genera of legumes. Here we show that the nodulation genes of this bacterium determine the production of a large family of Nod-factors which are N-acylated chitin pentamers carrying a variety of substituents. The terminal non-reducing glucosamine is N-acylated with vaccenic or palmitic acids, is N-methylated, and carries varying numbers of carbamoyl groups. The reducing N-acetyl-glucosamine residue is substituted on position 6 with 2-O-methyl-L-fucose which may be acetylated or sulphated or non-substituted. All three internal residues are N-acetylated. At pico- to nanomolar concentrations, these signal molecules exhibit biological activities on the tropical legumes Macroptilium and Vigna (Phaseoleae), as well as on both the temperate genera Medicago (Trifoliae) and Vicia (Viciae). These data strongly suggest that the uniquely broad host range of NGR234 is mediated by the synthesis of a family of varied sulphated and non-sulphated lipo-oligosaccharide signals.

Published
1992

25. Nodrm-1, a Sulphated Lipo-Oligosaccharide Signal of Rhizobium Meliloti Elicits Hair Deformation, Cortical Cell Division and Nodule Organogenesis on Alfalfa Roots

Author

Philippe Roche, F. de Billy, Jacques Vasse, Jean Dénarié, Fabienne Maillet, Patrice Lerouge, Georges Truchet, Catherine Faucher, Sylvie Camut, and Jean-Claude Promé

Subjects
Mutant, food and beverages, Organogenesis, Root hair, Biology, biology.organism_classification, Cell biology, chemistry.chemical_compound, chemistry, Glucosamine, Botany, Tetrasaccharide, Rhizobium, Gene, Function (biology)
Abstract

We have addressed the questions of how nodulation (nod) genes of the symbiotic bacterium R. meliloti operate to determine host specificity, plant (alfalfa) infection and nodulation. Using a root hair deformation assay we have shown that the common nodABC genes and the hostrange nodH and nodQ genes are all involved in the production of an extracellular signal. The structure of the major alfalfa-specific signal, NodRm-1, has been determined by mass spectrometry, NMR spectroscopy, radioactive labelling and chemical modifications. This signal is a sulphated and acylated glucosamine tetrasaccharide. NodRm-1 elicits root hair deformation, cortical cell divisions and nodule formation, on aseptically-grown alfalfa seedlings, at nanomolar concentrations. Hostrange nodH or nodQ mutants are able to infect a non-homologous host, common vetch and were found to excrete another signal, NodRm-2, which differs from NodRm-1 by the absence of the sulphate group. Purified NodRm-2 elicits hair deformation on vetch but not on alfalfa. The function of nodH and nodQ is to make the signal alfalfa-specific by transfer of a sulphate group. We propose that the nod genes of R.meliloti determine host specificity, root hair curling and nodule formation via the production of NodRm-1.

Published
1991
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26. An Extracellular Oligosaccharide Symbiotic Signal Produced by Rhizobium Meliloti

Author

Jean Dénarié, David G. Barker, Georges Truchet, Patrice Lerouge, Catherine Faucher, Jean-Claude Promé, Fabienne Maillet, and Philippe Roche

Subjects
chemistry.chemical_classification, Root nodule, biology, Plant morphogenesis, fungi, food and beverages, Root hair, Oligosaccharide, biology.organism_classification, Cell biology, Molecular level, chemistry, Symbiosis, Extracellular, Rhizobium
Abstract

The infection of leguminous plants by Rhizobiwn and the subsequent codifferentiation of both organisms leads ultimately to the formation of the unique nitrogen-fixing plant organ known as the root nodule. Within the nodule the Rhizobium are furnished with photosynthate-derived energy and, in exchange, the endosymbiotic bacterium reduces atmospheric nitrogen to a form which can be assimilated by the host plant. This remarkable symbiosis has been the subject of extensive research for many years, but it is only recently that it has become possible to study, at the molecular level, the role of diffusible factors in plant-bacterial signalling and recognition, with the exciting prospect that such molecules might also be responsible for triggering plant morphogenesis.

Published
1991
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27. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals

Author

Frédéric Debellé, Georges Truchet, Jean-Claude Promé, Jean Dénarié, Catherine Faucher, Philippe Roche, Fabienne Maillet, Patrice Lerouge, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, Centre National de la Recherche Scientifique (CNRS)-Institut National de la Recherche Agronomique (INRA), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and ProdInra, Migration

Subjects
Lipopolysaccharides, Rhizobiaceae, Root nodule, RELATION PLANTE MICROORGANISME, [SDV]Life Sciences [q-bio], Molecular Sequence Data, Restriction Mapping, Root hair, General Biochemistry, Genetics and Molecular Biology, Microbiology, Nod factor, 03 medical and health sciences, chemistry.chemical_compound, Sulfation, Glucosamine, Amino Acid Sequence, Cloning, Molecular, Symbiosis, 030304 developmental biology, 0303 health sciences, biology, 030306 microbiology, Sulfates, food and beverages, BIOLOGIE MOLECULAIRE, biology.organism_classification, FACTEUR NODE, [SDV] Life Sciences [q-bio], Biochemistry, chemistry, Genes, Bacterial, Azorhizobium, Rhizobium, Sulfotransferases, Sequence Alignment, Medicago sativa
Abstract

The symbiosis between Rhizobium and legumes is highly specific. For example, R. meliloti elicits the formation of root nodules on alfalfa and not on vetch. We recently reported that R. meliloti nodulation (nod) genes determine the production of acylated and sulfated glucosamine oligosaccharide signals. We now show that the biochemical function of the major host-range genes, nodH and nodPQ, is to specify the 6-O-sulfation of the reducing terminal glucosamine. Purified Nod factors (sulfated or not) from nodH+ or nodH- strains exhibited the same plant specificity in a variety of bioassays (root hair deformations, nodulation, changes in root morphology) as the bacterial cells from which they were purified. These results provide strong evidence that the molecular mechanism by which the nodH and nodPQ genes mediate host specificity is by determining the sulfation of the extracellular Nod signals.

Published
1991

28. Rhizobium meliloti nodulation genes specify the production of an alfalfa-specific sulfated lipo-oligosaccharide signal

Author

Françoise de Billy, Catherine Faucher, Fabienne Maillet, George Truchet, Jacques Vasse, Sylvie Camut, Patrice Lerouge, David G. Barker, Jean-Claude Promé, Jean Dénarié, and Philippe Roche

Subjects
Root nodule, fungi, food and beverages, Root hair, Biology, biology.organism_classification, Microbiology, Sulfation, Symbiosis, Biochemistry, Lipo oligosaccharide, Nitrogen fixation, Rhizobium, Gene
Abstract

The infection of leguminous plants by Rhizobium and the subsequent co-differentiation of both organisms leads ultimately to the formation of the unique nitrogen-fixing plant organ known as the root nodule (16). Within the nodule, the Rhizobium are furnished with photosynthate-derived energy and, in exchange, the endosymbiotic bacterium reduces atmospheric nitrogen to a form which can be assimilated by the host plant. This remarkable symbiosis has been the subject of extensive research for many years, but it is only recently that it has become possible to study, at the molecular level, the role of diffusible factors in plant-bacterial signalling and recognition, with the exciting prospect that such molecules might also be responsible for triggering plant morphogenesis.

Published
1990
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29. Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway

Author

Romy Catoira, R. Varma Penmetsa, Clare Gough, Charles Rosenberg, Jean Dénarié, Christine Galera, Françoise de Billy, Douglas R. Cook, Fabienne Maillet, and Etienne-Pascal Journet

Subjects
Mutant, Nod, Plant Science, Root hair, Genes, Plant, Plant Roots, Nod factor, Transduction (genetics), Gene Expression Regulation, Plant, Symbiosis, In Situ Hybridization, Plant Proteins, Genetics, biology, Genetic Complementation Test, Membrane Proteins, Cell Biology, biology.organism_classification, Medicago truncatula, Phenotype, RNA, Plant, Mutation, Rhizobium, Signal transduction, Medicago sativa, Signal Transduction, Research Article
Abstract

Rhizobium nodulation (Nod) factors are lipo-chitooligosaccharides that act as symbiotic signals, eliciting several key developmental responses in the roots of legume hosts. Using nodulation-defective mutants of Medicago truncatula, we have started to dissect the genetic control of Nod factor transduction. Mutants in four genes (DMI1, DMI2, DMI3, and NSP) were pleiotropically affected in Nod factor responses, indicating that these genes are required for a Nod factor–activated signal transduction pathway that leads to symbiotic responses such as root hair deformations, expressions of nodulin genes, and cortical cell divisions. Mutant analysis also provides evidence that Nod factors have a dual effect on the growth of root hair: inhibition of endogenous (plant) tip growth, and elicitation of a novel tip growth dependent on (bacterial) Nod factors. dmi1, dmi2, and dmi3 mutants are also unable to establish a symbiotic association with endomycorrhizal fungi, indicating that there are at least three common steps to nodulation and endomycorrhization in M. truncatula and providing further evidence for a common signaling pathway between nodulation and mycorrhization.

Published
2000
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30. The Rhizobium meliloti host range nodQ gene encodes a protein which shares homology with translation elongation and initiation factors

Author

Jacques Vasse, Emilio Cervantes, Fabienne Maillet, S. B. Sharma, Charles Rosenberg, and G. Truchet

Subjects
DNA, Bacterial, Molecular Sequence Data, Restriction Mapping, Biology, Microbiology, Eukaryotic translation, Bacterial Proteins, Peptide Initiation Factors, Consensus sequence, Initiation factor, Amino Acid Sequence, Molecular Biology, Peptide sequence, Gene, Genes, Dominant, Genetics, Base Sequence, Nucleic acid sequence, food and beverages, biochemical phenomena, metabolism, and nutrition, Peptide Elongation Factors, biology.organism_classification, Elongation factor, Genes, Bacterial, Conjugation, Genetic, Mutation, DNA Transposable Elements, bacteria, Rhizobium, Plasmids
Abstract

The Rhizobium meliloti nod region IIb is involved in host-range determination: (i) the presence of region IIb is necessary for transfer of alfalfa root hair curling ability to Rhizobium leguminosarum biovar trifolii; (ii) a mutation in region IIb extends the R. meliloti infection host range to Vicia sativa nigra; (iii) dominance of R. meliloti nod genes over R. leguminosarum biovar viciae nod genes is abolished by mutations in region IIb. The nucleotide sequence of this region has been determined. Genes corresponding to the two open reading frames identified are designated nodP and nodQ. The predicted amino acid sequence of the NodQ protein shows homology with translation initiation and elongation factors. The consensus sequence involved in the GTP-binding domain is conserved.

Published
1989
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31. Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal

Author

A. A. N. Van Brussel, Charles Rosenberg, Fabienne Maillet, C. Faucher, Jacques Vasse, G. Truchet, Jean Dénarié, Laboratoire de Biologie moléculaire des relations plantes-microorganismes, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), and ProdInra, Migration

Subjects
Rhizobiaceae, Genotype, Operon, Mutant, Root hair, Microbiology, Gene product, 03 medical and health sciences, Species Specificity, Gene expression, Botany, Extracellular, Escherichia coli, [SDV.MP] Life Sciences [q-bio]/Microbiology and Parasitology, Molecular Biology, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, biology, BIOCHIMIE, 030306 microbiology, INDUCTION, food and beverages, Plants, biology.organism_classification, Cell biology, Phenotype, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Genes, Bacterial, Rhizobium, Research Article, Plasmids
Abstract

The Rhizobium meliloti nodH gene is involved in determining host range specificity. By comparison with the wild-type strain, NodH mutants exhibit a change in host specificity. That is, although NodH mutants lose the ability to elicit root hair curling (Hac-), infection threads (Inf-), and nodule meristem formation (Nod-) on the homologous host alfalfa, they gain the ability to be Hac+ Inf+ Nod+ on a nonhomologous host such as common vetch. Using root hair deformation (Had) bioassays on alfalfa and vetch, we have demonstrated that sterile supernatant solutions of R. meliloti cultures, in which the nod genes had been induced by the plant flavone luteolin, contained symbiotic extracellular signals. The wild-type strain produced at least one Had signal active on alfalfa (HadA). The NodH- mutants did not produce this signal but produced at least one factor active on vetch (HadV). Mutants altered in the common nodABC genes produced neither of the Had factors. This result suggests that the nodABC operon determines the production of a common symbiotic factor which is modified by the NodH product into an alfalfa-specific signal. An absolute correlation was observed between the specificity of the symbiotic behavior of rhizobial cells and the Had specificity of their sterile filtrates. This indicates that the R. meliloti nodH gene determines host range by helping to mediate the production of a specific extracellular signal.

Published
1988

32. Respective Roles of Common and Specific Rhizobium meliloti nod Genes in the Control of Lucerne Infection

Author

Charles Rosenberg, Jean Dénarié, Georges Truchet, Fabienne Maillet, Frédéric Debellé, Jacques Vasse, and S. B. Sharma

Subjects
Rhizobiaceae, Medicago, Trigonella, Root nodule, biology, fungi, food and beverages, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, Rhizobia, Symbiosis, Botany, Rhizobium, Melilotus
Abstract

Rhizobia are soil bacteria which can infect specifically the roots of leguminous hosts and elicit the formation of root nodules in which they reduce dinitrogen into ammonia. The degree of specificity of this relationship is extremely varied. Some tropical strains can nodulate and fix nitrogen on a large number of genera belonging to various tribes of Leguminosae and even on the non-legume genus Parasponia. On the other hand Rhizobium meliloti strains are reported to have a very limited host range : each strain can nodulate effectively only some species of Medicago, Melilotus and Trigonella (see the review of Long 1984). R. meliloti is thus a suitable organism with which to investigate the genetic and molecular basis of a highly specific plant-bacteria interaction.

Published
1986
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33. Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with alpha,beta-unsaturated N-acyl substitutions

Author

Kristina Lindström, Frédéric Debellé, Michel Treilhou, Guo-Ping Yang, Odile Schiltz, Jean Dénarié, Fabienne Maillet, Myriam Ferro, Jean-Claude Promé, Corinne Vialas, Arlette Savagnac, and Danielle Promé

Subjects
Lipopolysaccharides, Rhizobiaceae, Glycosylation, Magnetic Resonance Spectroscopy, Acylation, Molecular Sequence Data, Microbiology, Plant Roots, Mass Spectrometry, Rhizobia, Rhizobium galegae, Nod factor, Nitrogen Fixation, Molecular Biology, Phylogeny, chemistry.chemical_classification, Plants, Medicinal, biology, Trifolieae, food and beverages, Fatty acid, Fabaceae, biology.organism_classification, chemistry, Carbohydrate Sequence, Fatty Acids, Unsaturated, Rhizobium, lipids (amino acids, peptides, and proteins)
Abstract

Rhizobia are symbiotic bacteria that synthesize lipochitooligosaccharide Nod factors (NFs), which act as signal molecules in the nodulation of specific legume hosts. Based on the structure of their N-acyl chain, NFs can be classified into two categories: (i) those that are acylated with fatty acids from the general lipid metabolism; and (ii) those (= alphaU-NFs) that are acylated by specific alpha,beta-unsaturated fatty acids (containing carbonyl-conjugated unsaturation(s)). Previous work has described how rhizobia that nodulate legumes of the Trifolieae and Vicieae tribes produce alphaU-NFs. Here, we have studied the structure of NFs from two rhizobial species that nodulate important genera of the Galegeae tribe, related to Trifolieae and Vicieae. Three strains of Mesorhizobium huakuii, symbionts of Astragalus sinicus, produced as major NFs, pentameric lipochitooligosaccharides O-sulphated and partially N-glycolylated at the reducing end and N-acylated, at the non-reducing end, by a C18:4 fatty acid. Two strains of Rhizobium galegae, symbionts of Galega sp., produced as major NFs, tetrameric O-carbamoylated NFs that could be O-acetylated on the glucosamine residue next to the non-reducing terminal glucosamine and were N-acylated by C18 and C20 alpha,beta-unsaturated fatty acids. These results suggest that legumes nodulated by rhizobia synthesizing alphaU-NFs constitute a phylogenetic cluster in the Galegoid phylum.

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