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1. A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses

Author

Brottier, Laurent, Chaintreuil, Clémence, Simion, Paul, Scornavacca, Céline, Rivallan, Ronan, Mournet, Pierre, Moulin, Lionel, Lewis, Gwilym P., Fardoux, Joël, Brown, Spencer C., Gomez-Pacheco, Mario, Bourges, Mickaël, Hervouet, Catherine, Gueye, Mathieu, Duponnois, Robin, Ramanankierana, Heriniaina, Randriambanona, Herizo, Vandrot, Hervé, Zabaleta, Maria, DasGupta, Maitrayee, D’Hont, Angélique, Giraud, Eric, and Arrighi, Jean-François

Published
2018
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2. Naturally occurring variations in the nod-independent model legume Aeschynomene evenia and relatives: a resource for nodulation genetics

Author

Chaintreuil, Clémence, Perrier, Xavier, Martin, Guillaume, Fardoux, Joël, Lewis, Gwilym P., Brottier, Laurent, Rivallan, Ronan, Gomez-Pacheco, Mario, Bourges, Mickaël, Lamy, Léo, Thibaud, Béatrice, Ramanankierana, Heriniaina, Randriambanona, Herizo, Vandrot, Hervé, Mournet, Pierre, Giraud, Eric, and Arrighi, Jean-François

Published
2018
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3. Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium-legume symbiosis

Author

Quilbé, Johan, Lamy, Léo, Brottier, Laurent, Leleux, Philippe, Fardoux, Joël, Rivallan, Ronan, Benichou, Thomas, Guyonnet, Rémi, Becana, Manuel, Villar, Irene, Garsmeur, Olivier, Hufnagel, Barbara, Delteil, Amandine, Gully, Djamel, Chaintreuil, Clémence, Pervent, Marjorie, Cartieaux, Fabienne, Bourge, Mickael, Valentin, Nicolas, Martin, Guillaume, Fontaine, Loïc, Droc, Gaëtan, Dereeper, Alexis, Farmer, Andrew, Libourel, Cyril, Nouwen, Nico, Gressent, Frédéric, Mournet, Pierre, D'Hont, Angélique, Giraud, Eric, Klopp, Christophe, Arrighi, Jean-François, Laboratoire des symbioses tropicales et méditerranéennes (UMR LSTM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-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)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Unité de Biométrie et Intelligence Artificielle de Toulouse [Castanet-Tolosan] (UBIA), Plateforme bioinformatique du GIS GENOTOUL - Génopole Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Amélioration génétique et adaptation des plantes méditerranéennes et tropicales (UMR AGAP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Département Systèmes Biologiques (Cirad-BIOS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Estación Experimental de Aula Dei (EEAD), Consejo Superior de Investigaciones Científicas [Madrid] (CSIC), Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Cytométrie (CYTO), Département Plateforme (PF I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Biologie et Génétique des Interactions Plante-Parasite (UMR BGPI), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), National center for genome resources (NCGR), 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), Spanish Ministry of Science and Innovation-European Regional Development Fund (AGL2017-85775-R), ANR-14-CE19-0005,AeschyNod,Génétique de la légumineuse Nod-indépendante Aeschynomene evenia pour étudier l'évolution de la symbiose rhizobienne et dans la perspective du transfert de la fixation d'azote aux plantes d'intérêt agronomique(2014), ANR-10-LABX-0001,AGRO,Agricultural Sciences for sustainable Development(2010), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - 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), Unité de Biométrie et Intelligence Artificielle (ancêtre de MIAT) (UBIA), Institut National de la Recherche Agronomique (INRA), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro, Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Plant Health Institute of Montpellier (UMR PHIM), and Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Agricultural genetics, Plant genetics, F60 - Physiologie et biochimie végétale, [SDV]Life Sciences [q-bio], Symbiose, nodosité racinaire, Plant Root Nodulation, Plant Roots, Article, F30 - Génétique et amélioration des plantes, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, Gene Expression Regulation, Plant, Légumineuse, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Amino Acid Sequence, Bradyrhizobium, Photosynthesis, Symbiosis, Phylogeny, Plant Proteins, Rhizobial symbiosis, Plant Stems, Formation de nodosités, phytogénétique, High-Throughput Nucleotide Sequencing, Fabaceae, Molecular Sequence Annotation, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, Biological Evolution, Aeschynomène, Gene Ontology, Transcriptome, Genome, Plant, Rhizobium, Signal Transduction, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Among legumes (Fabaceae) capable of nitrogen-fixing nodulation, several Aeschynomene spp. use a unique symbiotic process that is independent of Nod factors and infection threads. They are also distinctive in developing root and stem nodules with photosynthetic bradyrhizobia. Despite the significance of these symbiotic features, their understanding remains limited. To overcome such limitations, we conduct genetic studies of nodulation in Aeschynomene evenia, supported by the development of a genome sequence for A. evenia and transcriptomic resources for 10 additional Aeschynomene spp. Comparative analysis of symbiotic genes substantiates singular mechanisms in the early and late nodulation steps. A forward genetic screen also shows that AeCRK, coding a receptor-like kinase, and the symbiotic signaling genes AePOLLUX, AeCCamK, AeCYCLOPS, AeNSP2, and AeNIN are required to trigger both root and stem nodulation. This work demonstrates the utility of the A. evenia model and provides a cornerstone to unravel mechanisms underlying the rhizobium–legume symbiosis., The establishment of symbiotic interaction between Aeschynomene evenia and photosynthetic bradyrhizobia doesn’t involve the canonical Nod factors and infection threads. Here, the authors assemble the draft genome of A. evenia and identify a receptor-like kinase in mediating the symbiotic interaction.

Published
2021
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4. The Very Long Chain Fatty Acid (C26:25OH) Linked to the Lipid A Is Important for the Fitness of the Photosynthetic Bradyrhizobium Strain ORS278 and the Establishment of a Successful Symbiosis with Aeschynomene Legumes

Author

Busset, Nicolas, Di Lorenzo, Flaviana, Palmigiano, Angelo, Sturiale, Luisa, Gressent, Frédéric, Fardoux, Joel, Gully, Djamel, Chaintreuil, Clémence, Molinaro, Antonio, Silipo, Alba, 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), 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), Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant’Angelo, Università degli studi di Napoli Federico II, Consiglio Nazionale delle Ricerche (CNR), ANR-13-BSV7-0013,BugsInACell,Accommodation intracellulaire des bactéries symbiotiques fixatrices d'azote(2013), Giraud, Eric, University of Naples Federico II = Università degli studi di Napoli Federico II, and National Research Council of Italy | Consiglio Nazionale delle Ricerche (CNR)

Subjects
acide gras, Biodiversité et Ecologie, VLCFA, lipid A, Bradyrhizobium, acyltransferase, symbiosis, Aeschynomene, cluster de gènes, Biodiversity and Ecology, rhizobium, fixation de l'azote, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, symbiose, membrane externe
Abstract

International audience; In rhizobium strains, the lipid A is modified by the addition of a very long-chain fatty acid (VLCFA) shown to play an important role in rigidification of the outer membrane, thereby facilitating their dual life cycle, outside and inside the plant. In Bradyrhizobium strains, the lipid A is more complex with the presence of at least two VLCFAs, one covalently linked to a hopanoid molecule, but the importance of these modifications is not well-understood. In this study, we identified a cluster of VLCFA genes in the photosynthetic Bradyrhizobium strain ORS278, which nodulates Aeschynomene plants in a Nod factor-independent process. We tried to mutate the different genes of the VLCFA gene cluster to prevent the synthesis of the VLCFAs, but only one mutant in the lpxXL gene encoding an acyltransferase was obtained. Structural analysis of the lipid A showed that LpxXL is involved in the transfer of the C-26:25OH VLCFA to the lipid A but not in the one of the C30:29OH VLCFA which harbors the hopanoid molecule. Despite maintaining the second VLCFA, the ability of the mutant to cope with various stresses (low pH, high temperature, high osmolarity, and antimicrobial peptides) and to establish an efficient nitrogen-fixing symbiosis was drastically reduced. In parallel, we investigated whether the BRADO0045 gene, which encodes a putative acyltransferase displaying a weak identity with the apo-lipoprotein N-acyltransferase Lnt, could be involved in the transfer of the C-30:29OH VLCFA to the lipid A. Although the mutant exhibited phenotypes similar to the lpxXL mutant, no difference in the lipid A structure was observed from that in the wild-type strain, indicating that this gene is not involved in the modification of lipid A. Our results advance our knowledge of the biosynthesis pathway and the role of VLCFAs-modified lipid A in free-living and symbiotic states of Bradyrhizobium strains.

Published
2017
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5. The evolutionary dynamics of ancient and recent polyploidy in the African semiaquatic species of the legume genus Aeschynomene.

Author

Chaintreuil, Clémence, Gully, Djamel, Hervouet, Catherine, Tittabutr, Panlada, Randriambanona, Herizo, Brown, Spencer C., Lewis, Gwilym P., Bourge, Mickaël, Cartieaux, Fabienne, Boursot, Marc, Ramanankierana, Heriniaina, D'Hont, Angélique, Teaumroong, Neung, Giraud, Eric, and Arrighi, Jean‐François

Subjects
*AESCHYNOMENE, *GENOMES, *PLANT stems, *SYMBIOSIS, *NITROGEN
Abstract

The legume genus Aeschynomene is notable in the ability of certain semiaquatic species to develop nitrogen-fixing stem nodules. These species are distributed in two clades. In the first clade, all the species are characterized by the use of a unique Nod-independent symbiotic process. In the second clade, the species use a Nod-dependent symbiotic process and some of them display a profuse stem nodulation as exemplified in the African Aeschynomene afraspera., To facilitate the molecular analysis of the symbiotic characteristics of such legumes, we took an integrated molecular and cytogenetic approach to track occurrences of polyploidy events and to analyze their impact on the evolution of the African species of Aeschynomene., Our results revealed two rounds of polyploidy: a paleopolyploid event predating the African group and two neopolyploid speciations, along with significant chromosomal variations. Hence, we found that A. afraspera (8x) has inherited the contrasted genomic properties and the stem-nodulation habit of its parental lineages (4x)., This study reveals a comprehensive picture of African Aeschynomene diversification. It notably evidences a history that is distinct from the diploid Nod-independent clade, providing clues for the identification of the specific determinants of the Nod-dependent and Nod-independent symbiotic processes, and for comparative analysis of stem nodulation. [ABSTRACT FROM AUTHOR]

Published
2016
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6. The LPS O-Antigen in Photosynthetic Bradyrhizobium Strains Is Dispensable for the Establishment of a Successful Symbiosis with Aeschynomene Legumes.

Author

Busset, Nicolas, De Felice, Antonia, Chaintreuil, Clémence, Gully, Djamel, Fardoux, Joël, Romdhane, Sana, Molinaro, Antonio, Silipo, Alba, and Giraud, Eric

Subjects
BRADYRHIZOBIUM, SYMBIOSIS, AESCHYNOMENE, NITROGEN-fixing plants, PLANT species, PHOTOSYNTHETIC bacteria, LIPOPOLYSACCHARIDES
Abstract

The photosynthetic bradyrhizobia are able to use a Nod-factor independent process to induce nitrogen-fixing nodules on some semi-aquatic Aeschynomene species. These bacteria display a unique LPS O-antigen composed of a new sugar, the bradyrhizose that is regarded as a key symbiotic factor due to its non-immunogenic character. In this study, to check this hypothesis, we isolated mutants affected in the O-antigen synthesis by screening a transposon mutant library of the ORS285 strain for clones altered in colony morphology. Over the 10,000 mutants screened, five were selected and found to be mutated in two genes, rfaL, encoding for a putative O-antigen ligase and gdh encoding for a putative dTDP-glucose 4,6-dehydratase. Biochemical analysis confirmed that the LPS of these mutants completely lack the O-antigen region. However, no effect of the mutations could be detected on the symbiotic properties of the mutants indicating that the O-antigen region of photosynthetic Bradyrhizobium strains is not required for the establishment of symbiosis with Aeschynomene. [ABSTRACT FROM AUTHOR]

Published
2016
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7. Convergent Evolution of Endosymbiont Differentiation in Dalbergioid and Inverted Repeat-Lacking Clade Legumes Mediated by Nodule-Specific Cysteine-Rich Peptides.

Author

Czernic, Pierre, Gully, Djamel, Cartieaux, Fabienne, Moulin, Lionel, Guefrachi, Ibtissem, Patrel, Delphine, Pierre, Olivier, Fardoux, Joël, Chaintreuil, Clémence, Phuong Nguyen, Gressent, Frédéric, Da Silva, Corinne, Poulain, Julie, Wincker, Patrick, Rofidal, Valérie, Hem, Sonia, Barrière, Quentin, Arrighi, Jean-François, Mergaert, Peter, and Giraud, Eric

Subjects
LEGUMES, CYSTEINE, PEPTIDES, AESCHYNOMENE, POLYPLOIDY in plant chromosomes
Abstract

Nutritional symbiotic interactions require the housing of large numbers of microbial symbionts, which produce essential compounds for the growth of the host. In the legume-rhizobium nitrogen-fixing symbiosis, thousands of rhizobium microsymbionts, called bacteroids, are confined intracellularly within highly specialized symbiotic host cells. In Inverted Repeat-Lacking Clade (IRLC) legumes such as Medicago spp., the bacteroids are kept under control by an arsenal of nodulespecific cysteine-rich (NCR) peptides, which induce the bacteria in an irreversible, strongly elongated, and polyploid state. Here, we show that in Aeschynomene spp. legumes belonging to the more ancient Dalbergioid lineage, bacteroids are elongated or spherical depending on the Aeschynomene spp. and that these bacteroids are terminally differentiated and polyploid, similar to bacteroids in IRLC legumes. Transcriptome, in situ hybridization, and proteome analyses demonstrated that the symbiotic cells in the Aeschynomene spp. nodules produce a large diversity of NCR-like peptides, which are transported to the bacteroids. Blocking NCR transport by RNA interference-mediated inactivation of the secretory pathway inhibits bacteroid differentiation. Together, our results support the view that bacteroid differentiation in the Dalbergioid clade, which likely evolved independently from the bacteroid differentiation in the IRLC clade, is based on very similar mechanisms used by IRLC legumes. [ABSTRACT FROM AUTHOR]

Published
2015
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8. Radiation of the Nod-independent Aeschynomene relies on multiple allopolyploid speciation events.

Author

Arrighi, Jean‐François, Chaintreuil, Clémence, Cartieaux, Fabienne, Cardi, C., Rodier‐Goud, M., Brown, Spencer C., Boursot, Marc, D'Hont, Angélique, Dreyfus, Bernard, and Giraud, Eric

Subjects
*AESCHYNOMENE, *ALLOPOLYPLOIDY in plant chromosomes, *SYMBIOSIS, *FLOW cytometry, *PLANT phylogeny, *PLANT evolution
Abstract

The semi-aquatic legumes belonging to the genus Aeschynomene constitute a premium system for investigating the origin and evolution of unusual symbiotic features such as stem nodulation and the presence of a Nod-independent infection process. This latter apparently arose in a single Aeschynomene lineage. But how this unique Nod-independent group then radiated is not yet known., We have investigated the role of polyploidy in Aeschynomene speciation via a case study of the pantropical A. indica and then extended the analysis to the other Nod-independent species. For this, we combined SSR genotyping, genome characterization through flow cytometry, chromosome counting, FISH and GISH experiments, molecular phylogenies using ITS and single nuclear gene sequences, and artificial hybridizations., These analyses demonstrate the existence of an A. indica polyploid species complex comprising A. evenia (C. Wright) (2 n = 2x = 20), A. indica L. s.s. (2 n = 4x = 40) and a new hexaploid form (2 n = 6x = 60). This latter contains the two genomes present in the tetraploid ( A. evenia and A. scabra) and another unidentified genome. Two other species, A. pratensis and A. virginica, are also shown to be of allopolyploid origin., This work reveals multiple hybridization/polyploidization events, thus highlighting a prominent role of allopolyploidy in the radiation of the Nod-independent Aeschynomene. [ABSTRACT FROM AUTHOR]

Published
2014
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9. A Proteomic Approach of Bradyrhizobium/Aeschynomene Root and Stem Symbioses Reveals the Importance of the fixA Locus for Symbiosis.

Author

Delmotte, Nathanael, Mondy, Samuel, Alunni, Benoit, Fardoux, Joel, Chaintreuil, Clémence, Vorholt, Julia A., Giraud, Eric, and Gourion, Benjamin

Subjects
PROTEOMICS, BRADYRHIZOBIUM, AESCHYNOMENE, SYMBIOSIS, RHIZOBIACEAE, SOIL microbiology
Abstract

Rhizobia are soil bacteria that are able to form symbiosis with plant hosts of the legume family. These associations result in the formation of organs, called nodules in which bacteria fix atmospheric nitrogen to the benefit of the plant. Most of our knowledge on the metabolism and the physiology of the bacteria during symbiosis derives from studying roots nodules of terrestrial plants. Here we used a proteomics approach to investigate the bacterial physiology of photosynthetic Bradyrhizobium sp. ORS278 during the symbiotic process with the semi aquatical plant Aeschynomene indica that forms root and stem nodules. We analyzed the proteomes of bacteria extracted from each type of nodule. First, we analyzed the bacteroid proteome at two different time points and found only minor variation between the bacterial proteomes of 2-week- and 3-week-old nodules. High conservation of the bacteroid proteome was also found when comparing stem nodules and root nodules. Among the stem nodule specific proteins were those related to the phototrophic ability of Bradyrhizobium sp. ORS278. Furthermore, we compared our data with those obtained during an extensive genetic screen previously published. The symbiotic role of four candidate genes which corresponding proteins were found massively produced in the nodules but not identified during this screening was examined. Mutant analysis suggested that in addition to the EtfAB system, the fixA locus is required for symbiotic efficiency. [ABSTRACT FROM AUTHOR]

Published
2014
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10. Evolution of symbiosis in the legume genus Aeschynomene.

Author

Chaintreuil, Clémence, Arrighi, Jean‐François, Giraud, Eric, Miché, Lucie, Moulin, Lionel, Dreyfus, Bernard, Munive‐Hernández, José‐Antonio, Villegas‐Hernandez, María del Carmen, and Béna, Gilles

Subjects
*AESCHYNOMENE, *BRADYRHIZOBIUM, *DNA, *PHYLOGENY, *INTRONS
Abstract

Legumes in the genus Aeschynomene form nitrogen-fixing root nodules in association with Bradyrhizobium strains. Several aquatic and subaquatic species have the additional capacity to form stem nodules, and some of them can symbiotically interact with specific strains that do not produce the common Nod factors synthesized by all other rhizobia. The question of the emergence and evolution of these nodulation characters has been the subject of recent debate., We conducted a molecular phylogenetic analysis of 38 different Aeschynomene species. The phylogeny was reconstructed with both the chloroplast DNA trnL intron and the nuclear ribosomal DNA ITS/5.8 S region. We also tested 28 Aeschynomene species for their capacity to form root and stem nodules by inoculating different rhizobial strains, including nod ABC-containing strains ( ORS285, USDA110) and a nod ABC-lacking strain ( ORS278)., Maximum likelihood analyses resolved four distinct phylogenetic groups of Aeschynomene. We found that stem nodulation may have evolved several times in the genus, and that all Aeschynomene species using a Nod-independent symbiotic process clustered in the same clade., The phylogenetic approach suggested that Nod-independent nodulation has evolved once in this genus, and should be considered as a derived character, and this result is discussed with regard to previous experimental studies. [ABSTRACT FROM AUTHOR]

Published
2013
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11. Genotype Delimitation in the Nod-Independent Model Legume Aeschynomene evenia

Author

Arrighi, Jean-François, Cartieaux, Fabienne, Chaintreuil, Clémence, Brown, Spencer, Boursot, Marc, and Giraud, Eric

Subjects
AESCHYNOMENE, GENOTYPE-environment interaction, PLANT genetics, NITROGEN-fixing plants, MICROBIOLOGY, PLANTS, FLOW cytometry, PLANT classification
Abstract

Research on the nitrogen-fixing symbiosis has been so far focused on two model legumes, Medicago truncatula and Lotus japonicus, which use a sophisticated infection process involving infection thread formation. However, in 25% of the legumes, the bacterial entry occurs more simply in an intercellular fashion. Among them, some semi-aquatic Aeschynomene species present the distinctive feature to form nitrogen-fixing nodules on both roots and stems following elicitation by photosynthetic bradyrhizobia that do not produce Nod factors. This interaction is believed to represent a living testimony of the ancestral state of the rhizobium-legume symbiosis. To decipher the molecular mechanisms of this unique Nod-independent nitrogen-fixing symbiosis, we previously identified A. evenia C. Wright as an appropriate model legume, because it displays all the requisites for molecular and genetic approaches. To advance the use of this new model legume species, here we characterized the intraspecific diversity found in A. evenia. For this, the accessions available in germplasm banks were collected and subjected to morphological investigations, genotyping with RAPD and SSR markers, molecular phylogenies using ITS and single nuclear gene sequences, and cross-compatibility tests. These combined analyses revealed an important intraspecific differentiation that led us to propose a new taxonomic classification for A. evenia comprising two subspecies and four varieties. The A. evenia ssp. evenia contains var. evenia and var. pauciciliata whereas A. evenia ssp. serrulata comprises var. serrulata and var. major. This study provides information to exploit efficiently the diversity encountered in A. evenia and proposes subsp. evenia as the most appropriate subspecies for future projects aimed at identifying plant determinants of the Nod-independent symbiotic process. [ABSTRACT FROM AUTHOR]

Published
2013
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12. Diversity analyses of Aeschynomene symbionts in Tropical Africa and Central America reveal that nod-independent stem nodulation is not restricted to photosynthetic bradyrhizobia.

Author

Miché, Lucie, Moulin, Lionel, Chaintreuil, Clémence, Contreras-Jimenez, José Luis, Munive-Hernández, José-Antonio, del Carmen Villegas-Hernandez, María, Crozier, Françoise, and Béna, Gilles

Subjects
AESCHYNOMENE, LEGUMES, AQUATIC plants, PHOTOSYNTHETIC bacteria, RHIZOBIUM
Abstract

Tropical aquatic legumes of the genus Aeschynomene are unique in that they can be stem-nodulated by photosynthetic bradyrhizobia. Moreover, a recent study demonstrated that two Aeschynomene indica symbionts lack canonical nod genes, thereby raising questions about the distribution of such atypical symbioses among rhizobial–legume interactions. Population structure and genomic diversity were compared among stem-nodulating bradyrhizobia isolated from various Aeschynomene species of Central America and Tropical Africa. Phylogenetic analyses based on the recA gene and whole-genome amplified fragment length polymorphism (AFLP) fingerprints on 110 bacterial strains highlighted that all the photosynthetic strains form a separate cluster among bradyrhizobia, with no obvious structuring according to their geographical or plant origins. Nod-independent symbiosis was present in all sampling areas and seemed to be linked to Aeschynomene host species. However, it was not strictly dependent on photosynthetic ability, as exemplified by a newly identified cluster of strains that lacked canonical nod genes and efficiently stem-nodulated A. indica, but were not photosynthetic. Interestingly, the phenotypic properties of this new cluster of bacteria were reflected by their phylogenetical position, as being intermediate in distance between classical root-nodulating Bradyrhizobium spp. and photosynthetic ones. This result opens new prospects about stem-nodulating bradyrhizobial evolution. [ABSTRACT FROM AUTHOR]

Published
2010
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13. Naturally occurring variations in the nod-independent model legume <italic>Aeschynomene evenia</italic> and relatives: a resource for nodulation genetics.

Author

Chaintreuil, Clémence, Perrier, Xavier, Martin, Guillaume, Fardoux, Joël, Lewis, Gwilym P., Brottier, Laurent, Rivallan, Ronan, Gomez-Pacheco, Mario, Bourges, Mickaël, Lamy, Léo, Thibaud, Béatrice, Ramanankierana, Heriniaina, Randriambanona, Herizo, Vandrot, Hervé, Mournet, Pierre, Giraud, Eric, and Arrighi, Jean-François

Subjects
AESCHYNOMENE, LEGUMES, GENOTYPES, PLOIDY, SYMBIOSIS
Abstract

Background: Among semi-aquatic species of the legume genus Aeschynomene, some have the unique property of being root and stem-nodulated by photosynthetic Bradyrhizobium lacking the nodABC genes necessary for the production of Nod factors. These species provide an excellent biological system with which to explore the evolution of nodulation in legumes. Among them, Aeschynomene evenia has emerged as a model legume to undertake the genetic dissection of the so-called Nod-independent symbiosis. In addition to the genetic analysis of nodulation on a reference line, natural variation in a germplasm collection could also be surveyed to uncover genetic determinants of nodulation. To this aim, we investigated the patterns of genetic diversity in a collection of 226 Nod-independent Aeschynomene accessions. Results: A combination of phylogenetic analyses, comprising ITS and low-copy nuclear genes, along with cytogenetic experiments and artificial hybridizations revealed the richness of the Nod-independent Aeschynomene group with the identification of 13 diploid and 6 polyploid well-differentiated taxa. A set of 54 SSRs was used to further delineate taxon boundaries and to identify different genotypes. Patterns of microsatellite diversity also illuminated the genetic basis of the Aeschynomene taxa that were all found to be predominantly autogamous and with a predicted simple disomic inheritance, two attributes favorable for genetics. In addition, taxa displaying a pronounced genetic diversity, notably A. evenia, A. indica and A. sensitiva, were characterized by a clear geographically-based genetic structure and variations in root and stem nodulation. Conclusion: A well-characterized germplasm collection now exists as a major genetic resource to thoroughly explore the natural variation of nodulation in response to different bradyrhizobial strains. Symbiotic polymorphisms are expected to be found notably in the induction of nodulation, in nitrogen fixation and also in stem nodulation. Subsequent genetic analysis and locus mapping will pave the way for the identification of the underlying genes through forward or reverse genetics. Such discoveries will significantly contribute to our understanding of the molecular mechanisms underpinning how some Aeschynomene species can be efficiently nodulated in a Nod-independent fashion. [ABSTRACT FROM AUTHOR]

Published
2018
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14. Photosynthetic Bradyrhizobium sp. Strain 0RS285 Is Capable of Forming Nitrogen-Fixing Root Nodules on Soybeans (Glycine max).

Author

Giraud, Eric, Lei Xu, Chaintreuil, Clémence, Gargani, Daniel, Gully, Djamel, and Sadowsky, Michael J.

Subjects
*BRADYRHIZOBIUM japonicum, *SOYBEAN, *PHOTOSYNTHETIC bacteria, *AESCHYNOMENE, *NITROGEN fixation, *PLANT growth, *ROOT-tubercles
Abstract

The ability of photosynthetic Bradyrhizobium strains 0RS285 and 0RS278 to nodulate soybeans was investigated. While the nod gene-deficient 0RS278 strain induced bumps only on soybean roots, the nod gene-containing 0RS285 strain formed nitrogen-fixing nodules. However, symbiotic efficiencies differed drastically depending on both the soybean genotype used and the culture conditions tested. [ABSTRACT FROM AUTHOR]

Published
2013
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15. A Peptidoglycan-Remodeling Enzyme Is Critical for Bacteroid Differentiation in Bradyrhizobium spp. During Legume Symbiosis

Author

Daniel Gargani, Djamel Gully, Clémence Chaintreuil, Peter Mergaert, Katia Bonaldi, Joël Fardoux, Cédric Grangeteau, Roberta Marchetti, Eric Giraud, Nico Nouwen, Antonio Molinaro, Phuong Nguyen, 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), 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)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Center for Chronobiology, Division of Biological Sciences, University of California [San Diego] (UC San Diego), University of California-University of California, Vin Aliment Microbiologie et Stress (VAlMiS), Procédés Alimentaires et Microbiologiques (PAM), Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Procédés Alimentaires et Microbiologiques [Dijon] (PAM), Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC), Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant'Angelo, Università di Napoli Federico II, Intéractions Plantes-Bactéries (PBI), Département Microbiologie (Dpt Microbio), Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), 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 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), Université Bourgogne Franche-Comté [COMUE] (UBFC)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), ANR-13-BSV7-0013,BugsInACell,Accommodation intracellulaire des bactéries symbiotiques fixatrices d'azote(2013), University of California (UC)-University of California (UC), University of Naples Federico II = Università degli studi di Napoli Federico II, Laboratoire des symbioses tropicales et méditerranéennes ( LSTM ), Centre de Coopération Internationale en Recherche Agronomique pour le Développement ( CIRAD ) -Université Montpellier 1 ( UM1 ) -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 ), Biologie et Génétique des Interactions Plante-Parasite ( BGPI ), 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 ), University of California [San Diego] ( UC San Diego ), Vin Aliment Microbiologie et Stress ( VAlMiS ), Procédés Alimentaires et Microbiologiques ( PAM ), Université de Bourgogne ( UB ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université de Bourgogne ( UB ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Procédés Alimentaires et Microbiologiques [Dijon] ( PAM ), Université de Bourgogne ( UB ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté ( UBFC ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté ( UBFC ), Intéractions Plantes-Bactéries ( PBI ), Département Microbiologie ( Dpt Microbio ), Institut de Biologie Intégrative de la Cellule ( I2BC ), Université Paris-Sud - Paris 11 ( UP11 ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Université Paris-Sud - Paris 11 ( UP11 ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Institut de Biologie Intégrative de la Cellule ( I2BC ), Université Paris-Sud - Paris 11 ( UP11 ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Université Paris-Sud - Paris 11 ( UP11 ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ), Université Paris-Sud - Paris 11 ( UP11 ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ), Gully, Djamel, Gargani, Daniel, Bonaldi, Katia, Grangeteau, Cédric, Chaintreuil, Clémence, Fardoux, Joël, Nguyen, Phuong, Marchetti, Roberta, Nouwen, Nico, Molinaro, Antonio, Mergaert, Peter, and Giraud, Eric

Subjects
0301 basic medicine, Physiology, [SDV]Life Sciences [q-bio], Mutant, nodosité racinaire, chemistry.chemical_compound, Bacteroides, Bradyrhizobium, Photosynthesis, Photosynthèse, Différenciation cellulaire, 2. Zero hunger, food and beverages, Fabaceae, General Medicine, Polyploïdie, Code génétique, Rhizobium, Symbiosi, F60 - Physiologie et biochimie végétale, Symbiose, Bacterial Protein, Peptidoglycan, Biology, Microbiology, 03 medical and health sciences, Photosynthesi, Bacterial Proteins, Symbiosis, Peptidase, Binding Sites, [ SDV ] Life Sciences [q-bio], Binding Site, P34 - Biologie du sol, Aeschynomene, Gene Expression Regulation, Bacterial, biology.organism_classification, 030104 developmental biology, chemistry, Enzyme, Mutation, Agronomy and Crop Science, Bacteria
Abstract

International audience; In response to the presence of compatible rhizobium bacteria, legumes form symbiotic organs called nodules on their roots. These nodules house nitrogen-fixing bacteroids that are a differentiated form of the rhizobium bacteria. In some legumes, the bacteroid differentiation comprises a dramatic cell enlargement, polyploidization, and other morphological changes. Here, we demonstrate that a peptidoglycan-modifying enzyme in Bradyrhizobium strains, a DD-carboxypeptidase that contains a peptidoglycan-binding SPOR domain, is essential for normal bacteroid differentiation in Aeschynomene species. The corresponding mutants formed bacteroids that are malformed and hypertrophied. However, in soybean, a plant that does not induce morphological differentiation of its symbiont, the mutation does not affect the bacteroids. Remarkably, the mutation also leads to necrosis in a large fraction of the Aeschynomene nodules, indicating that a normally formed peptidoglycan layer is essential for avoiding the induction of plant immune responses by the invading bacteria. In addition to exopolysaccharides, capsular polysaccharides, and lipopolysaccharides, whose role during symbiosis is well defined, our work demonstrates an essential role in symbiosis for yet another rhizobial envelope component, the peptidoglycan layer.

Published
2016
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16. The LPS O-antigen in photosynthetic Bradyrhizobium strains Is dispensable for the establishment of a successful symbiosis with Aeschynomene legumes

Author

Alba Silipo, Eric Giraud, Sana Romdhane, Djamel Gully, Clémence Chaintreuil, Nicolas Busset, Antonia De Felice, Antonio Molinaro, 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), Dipartimento di Scienze Chimiche, Complesso Universitario Monte Sant’Angelo, Università degli studi di Napoli Federico II, Busset, Nicola, DE FELICE, Antonia, Chaintreuil, Clémence, Gully, Djamel, Fardoux, Joël, Romdhane, Sana, Molinaro, Antonio, Silipo, Alba, Giraud, Eric, University of Naples Federico II = Università degli studi di Napoli Federico II, and 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)

Subjects
0301 basic medicine, fixation d'azote, Biodiversité et Ecologie, Mutant, lcsh:Medicine, Biochemistry, biodiversité, Ligases, Mobile Genetic Elements, lcsh:Science, mutagenèse, Multidisciplinary, biology, Medicine (all), O Antigens, Fabaceae, Genomics, Plants, Legumes, symbiosis, Enzymes, Mutant Strains, symbiose, Research Article, Sugar Alcohol Dehydrogenases, Transposable element, nodule, Library Screening, Research and Analysis Methods, Bradyrhizobium, Microbiology, Biodiversity and Ecology, 03 medical and health sciences, Genetic Elements, Symbiosis, Bacterial Proteins, Botany, Genetics, Molecular Biology Techniques, Gene, Molecular Biology, Cloning, Molecular Biology Assays and Analysis Techniques, Biochemistry, Genetics and Molecular Biology (all), Bacteria, bradyrhizobium, lcsh:R, Organisms, Transposable Elements, Aeschynomene, Biology and Life Sciences, Proteins, biology.organism_classification, Species Interactions, 030104 developmental biology, Agricultural and Biological Sciences (all), Mutation, Enzymology, lcsh:Q, [SDE.BE]Environmental Sciences/Biodiversity and Ecology
Abstract

The photosynthetic bradyrhizobia are able to use a Nod-factor independent process to induce nitrogen-fixing nodules on some semi-aquatic Aeschynomene species. These bacteria display a unique LPS O-antigen composed of a new sugar, the bradyrhizose that is regarded as a key symbiotic factor due to its non-immunogenic character. In this study, to check this hypothesis, we isolated mutants affected in the O-antigen synthesis by screening a transposon mutant library of the ORS285 strain for clones altered in colony morphology. Over the 10,000 mutants screened, five were selected and found to be mutated in two genes, rfaL, encoding for a putative O-antigen ligase and gdh encoding for a putative dTDP-glucose 4,6-dehydratase. Biochemical analysis confirmed that the LPS of these mutants completely lack the O-antigen region. However, no effect of the mutations could be detected on the symbiotic properties of the mutants indicating that the O-antigen region of photosynthetic Bradyrhizobium strains is not required for the establishment of symbiosis with Aeschynomene.

Published
2016
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