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1. Versatility of Stenotrophomonas maltophilia: Ecological roles of RND efflux pumps

Author

Amandine Chauviat, Thibault Meyer, and Sabine Favre-Bonté

Subjects
Environmental resistance, Opportunistic pathogen, Ecological niche, Natural inducer, Regulatory pathway, Science (General), Q1-390, Social sciences (General), H1-99
Abstract

S. maltophilia is a widely distributed bacterium found in natural, anthropized and clinical environments. The genome of this opportunistic pathogen of environmental origin includes a large number of genes encoding RND efflux pumps independently of the clinical or environmental origin of the strains. These pumps have been historically associated with the uptake of antibiotics and clinically relevant molecules because they confer resistance to many antibiotics. However, considering the environmental origin of S. maltophilia, the ecological role of these pumps needs to be clarified. RND efflux systems are highly conserved within bacteria and encountered both in pathogenic and non-pathogenic species. Moreover, their evolutionary origin, conservation and multiple copies in bacterial genomes suggest a primordial role in cellular functions and environmental adaptation. This review is aimed at elucidating the ecological role of S. maltophilia RND efflux pumps in the environmental context and providing an exhaustive description of the environmental niches of S. maltophilia. By looking at the substrates and functions of the pumps, we propose different involvements and roles according to the adaptation of the bacterium to various niches. We highlight that i°) regulatory mechanisms and inducer molecules help to understand the conditions leading to their expression, and ii°) association and functional redundancy of RND pumps and other efflux systems demonstrate their complex role within S. maltophilia cells. These observations emphasize that RND efflux pumps play a role in the versatility of S. maltophilia.

Published
2023
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2. Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction

Author

Grégory Hoff, Anthony Arguelles Arias, Farah Boubsi, Jelena Pršić, Thibault Meyer, Heba M. M. Ibrahim, Sébastien Steels, Patricio Luzuriaga, Aurélien Legras, Laurent Franzil, Michelle Lequart-Pillon, Catherine Rayon, Victoria Osorio, Edwin de Pauw, Yannick Lara, Estelle Deboever, Barbara de Coninck, Philippe Jacques, Magali Deleu, Emmanuel Petit, Olivier Van Wuytswinkel, and Marc Ongena

Subjects
lipopeptides, plant cell wall polymers, plant immunity, molecular crosstalk, plant-microbe interactions, Microbiology, QR1-502
Abstract

ABSTRACT Bacillus velezensis is considered as a model species belonging to the so-called Bacillus subtilis complex that evolved typically to dwell in the soil rhizosphere niche and establish an intimate association with plant roots. This bacterium provides protection to its natural host against diseases and represents one of the most promising biocontrol agents. However, the molecular basis of the cross talk that this bacterium establishes with its natural host has been poorly investigated. We show here that these plant-associated bacteria have evolved a polymer-sensing system to perceive their host and that, in response, they increase the production of the surfactin-type lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favored upon growth on root exudates and that this lipopeptide is a key component used by the bacterium to optimize biofilm formation, motility, and early root colonization. In this specific nutritional context, the bacterium also modulates qualitatively the pattern of surfactin homologues coproduced in planta and forms mainly variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. IMPORTANCE Within the plant-associated microbiome, some bacterial species are of particular interest due to the disease protective effect they provide via direct pathogen suppression and/or stimulation of host immunity. While these biocontrol mechanisms are quite well characterized, we still poorly understand the molecular basis of the cross talk these beneficial bacteria initiate with their host. Here, we show that the model species Bacillus velezensis stimulates the production of the surfactin lipopeptide upon sensing pectin as a cell surface molecular pattern and upon feeding on root exudates. Surfactin favors bacterial rhizosphere fitness on one hand and primes the plant immune system on the other hand. Our data therefore illustrate how both partners use this multifunctional compound as a unique shared good to sustain a mutualistic interaction.

Published
2021
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3. Lipopeptide Interplay Mediates Molecular Interactions between Soil Bacilli and Pseudomonads

Author

Sofija Andrić, Thibault Meyer, Augustin Rigolet, Claire Prigent-Combaret, Monica Höfte, Guillaume Balleux, Sébastien Steels, Grégory Hoff, René De Mot, Andrea McCann, Edwin De Pauw, Anthony Argüelles Arias, and Marc Ongena

Subjects
Bacillus velezensis, molecular cross-talk, Pseudomonas, bioactive secondary metabolites, cyclic lipopeptides, microbial ecology, Microbiology, QR1-502
Abstract

ABSTRACT Some Bacillus species, such as B. velezensis, are important members of the plant-associated microbiome, conferring protection against phytopathogens. However, our knowledge about multitrophic interactions determining the ecological fitness of these biocontrol bacteria in the competitive rhizosphere niche is still limited. Here, we investigated molecular mechanisms underlying interactions between B. velezensis and Pseudomonas as a soil-dwelling competitor. Upon their contact-independent in vitro confrontation, a multifaceted macroscopic outcome was observed and characterized by Bacillus growth inhibition, white line formation in the interaction zone, and enhanced motility. We correlated these phenotypes with the production of bioactive secondary metabolites and identified specific lipopeptides as key compounds involved in the interference interaction and motile response. Bacillus mobilizes its lipopeptide surfactin not only to enhance motility but also to act as a chemical trap to reduce the toxicity of lipopeptides formed by Pseudomonas. We demonstrated the relevance of these unsuspected roles of lipopeptides in the context of competitive tomato root colonization by the two bacterial genera. IMPORTANCE Plant-associated Bacillus velezensis and Pseudomonas spp. represent excellent model species as strong producers of bioactive metabolites involved in phytopathogen inhibition and the elicitation of plant immunity. However, the ecological role of these metabolites during microbial interspecies interactions and the way their expression may be modulated under naturally competitive soil conditions has been poorly investigated. Through this work, we report various phenotypic outcomes from the interactions between B. velezensis and 10 Pseudomonas strains used as competitors and correlate them with the production of specific metabolites called lipopeptides from both species. More precisely, Bacillus overproduces surfactin to enhance motility, which also, by acting as a chemical trap, reduces the toxicity of other lipopeptides formed by Pseudomonas. Based on data from interspecies competition on plant roots, we assume this would allow Bacillus to gain fitness and persistence in its natural rhizosphere niche. The discovery of new ecological functions for Bacillus and Pseudomonas secondary metabolites is crucial to rationally design compatible consortia, more efficient than single-species inoculants, to promote plant health and growth by fighting economically important pathogens in sustainable agriculture.

Published
2021
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4. Bacillus Responses to Plant-Associated Fungal and Bacterial Communities

Author

Sofija Andrić, Thibault Meyer, and Marc Ongena

Subjects
Bacillus, rhizosphere, bioactive secondary metabolites, microbial interaction, biocontrol, molecular cross-talk, Microbiology, QR1-502
Abstract

Some members of root-associated Bacillus species have been developed as biocontrol agents due to their contribution to plant protection by directly interfering with the growth of pathogens or by stimulating systemic resistance in their host. As rhizosphere-dwelling bacteria, these bacilli are surrounded and constantly interacting with other microbes via different types of communications. With this review, we provide an updated vision of the molecular and phenotypic responses of Bacillus upon sensing other rhizosphere microorganisms and/or their metabolites. We illustrate how Bacillus spp. may react by modulating the production of secondary metabolites, such as cyclic lipopeptides or polyketides. On the other hand, some developmental processes, such as biofilm formation, motility, and sporulation may also be modified upon interaction, reflecting the adaptation of Bacillus multicellular communities to microbial competitors for preserving their ecological persistence. This review also points out the limited data available and a global lack of knowledge indicating that more research is needed in order to, not only better understand the ecology of bacilli in their natural soil niche, but also to better assess and improve their promising biocontrol potential.

Published
2020
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5. Ecological Conditions and Molecular Determinants Involved in Agrobacterium Lifestyle in Tumors

Author

Thibault Meyer, Clémence Thiour-Mauprivez, Florence Wisniewski-Dyé, Isabelle Kerzaon, Gilles Comte, Ludovic Vial, and Céline Lavire

Subjects
Agrobacterium tumefaciens, tumor lifestyle, crown gall, molecular traits, competition, plant defense, Plant culture, SB1-1110
Abstract

The study of pathogenic agents in their natural niches allows for a better understanding of disease persistence and dissemination. Bacteria belonging to the Agrobacterium genus are soil-borne and can colonize the rhizosphere. These bacteria are also well known as phytopathogens as they can cause tumors (crown gall disease) by transferring a DNA region (T-DNA) into a wide range of plants. Most reviews on Agrobacterium are focused on virulence determinants, T-DNA integration, bacterial and plant factors influencing the efficiency of genetic transformation. Recent research papers have focused on the plant tumor environment on the one hand, and genetic traits potentially involved in bacterium-plant interactions on the other hand. The present review gathers current knowledge about the special conditions encountered in the tumor environment along with the Agrobacterium genetic determinants putatively involved in bacterial persistence inside a tumor. By integrating recent metabolomic and transcriptomic studies, we describe how tumors develop and how Agrobacterium can maintain itself in this nutrient-rich but stressful and competitive environment.

Published
2019
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6. Bacillus Cyclic Lipopeptides Iturin and Fengycin Control Rice Blast Caused by Pyricularia oryzae in Potting and Acid Sulfate Soils by Direct Antagonism and Induced Systemic Resistance

Author

Van Bach Lam, Thibault Meyer, Anthony Arguelles Arias, Marc Ongena, Feyisara Eyiwumi Oni, and Monica Höfte

Subjects
Bacillus altitudinis, Bacillus velezensis, fengycin, iturin, surfactin, rice blast, Biology (General), QH301-705.5
Abstract

Rice monoculture in acid sulfate soils (ASSs) is affected by a wide range of abiotic and biotic constraints, including rice blast caused by Pyricularia oryzae. To progress towards a more sustainable agriculture, our research aimed to screen the biocontrol potential of indigenous Bacillus spp. against blast disease by triggering induced systemic resistance (ISR) via root application and direct antagonism. Strains belonging to the B. altitudinis and B. velezensis group could protect rice against blast disease by ISR. UPLC–MS and marker gene replacement methods were used to detect cyclic lipopeptide (CLiP) production and construct CLiPs deficient mutants of B. velezensis, respectively. Here we show that the CLiPs fengycin and iturin are both needed to elicit ISR against rice blast in potting soil and ASS conditions. The CLiPs surfactin, iturin and fengycin completely suppressed P. oryzae spore germination resulting in disease severity reduction when co-applied on rice leaves. In vitro microscopic assays revealed that iturin and fengycin inhibited the mycelial growth of the fungus P. oryzae, while surfactin had no effect. The capacity of indigenous Bacillus spp. to reduce rice blast by direct and indirect antagonism in ASS conditions provides an opportunity to explore their usage for rice blast control in the field.

Published
2021
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7. Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor

Author

Sofija Andrić, Augustin Rigolet, Anthony Argüelles Arias, Sébastien Steels, Grégory Hoff, Guillaume Balleux, Loïc Ongena, Monica Höfte, Thibault Meyer, and Marc Ongena

Subjects
Agriculture and Food Sciences, Biology and Life Sciences, SUBTILIS, Microbiology, GENE CLUSTERS, SOIL, PHENAZINES, SP CMR12A, RHIZOCTONIA ROOT-ROT, Earth and Environmental Sciences, NATURAL-PRODUCTS, GROWTH PROMOTION, BIOSYNTHESIS, BIOLOGICAL-CONTROL, Ecology, Evolution, Behavior and Systematics
Abstract

Bacillus velezensis is considered as model species for plant-associated bacilli providing benefits to its host such as protection against phytopathogens. This is mainly due to the potential to secrete a wide range of secondary metabolites with specific and complementary bioactivities. This metabolite arsenal has been quite well defined genetically and chemically but much remains to be explored regarding how it is expressed under natural conditions and notably how it can be modulated upon interspecies interactions in the competitive rhizosphere niche. Here, we show that B. velezensis can mobilize a substantial part of its metabolome upon the perception of Pseudomonas, as a soil-dwelling competitor. This metabolite response reflects a multimodal defensive strategy as it includes polyketides and the bacteriocin amylocyclicin, with broad antibiotic activity, as well as surfactin lipopeptides, contributing to biofilm formation and enhanced motility. Furthermore, we identified the secondary Pseudomonas siderophore pyochelin as an info-chemical, which triggers this response via a mechanism independent of iron stress. We hypothesize that B. velezensis relies on such chelator sensing to accurately identify competitors, illustrating a new facet of siderophore-mediated interactions beyond the concept of competition for iron and siderophore piracy. This phenomenon may thus represent a new component of the microbial conversations driving the behavior of members of the rhizosphere community.

Published
2022

8. Bacillus Cyclic Lipopeptides Iturin and Fengycin Control Rice Blast Caused by Pyricularia oryzae in Potting and Acid Sulfate Soils by Direct Antagonism and Induced Systemic Resistance

Author

Thibault Meyer, Feyisara Eyiwumi Oni, Monica Höfte, Marc Ongena, Van Bach Lam, Anthony Arguelles Arias, Universiteit Gent = Ghent University [Belgium] (UGENT), Université de Liège, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Résistance Induite et Bioprotection des Plantes - EA 4707 (RIBP), Université de Reims Champagne-Ardenne (URCA)-SFR Condorcet, and Université de Reims Champagne-Ardenne (URCA)-Université de Picardie Jules Verne (UPJV)-Centre National de la Recherche Scientifique (CNRS)-Université de Reims Champagne-Ardenne (URCA)-Université de Picardie Jules Verne (UPJV)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Agriculture and Food Sciences, 0106 biological sciences, 0301 basic medicine, Microbiology (medical), Pyricularia, acid sulfate soil, QH301-705.5, ved/biology.organism_classification_rank.species, BIOLOGY, Bacillus altitudinis, Fungus, Biology, SUBTILIS, 01 natural sciences, Microbiology, surfactin, Article, 03 medical and health sciences, chemistry.chemical_compound, PLANT INFECTION, Virology, Bacillus velezensis, Spore germination, Pyricularia oryzae, Biology (General), Mycelium, 2. Zero hunger, ved/biology, fengycin, rice blast, food and beverages, iturin, biology.organism_classification, Potting soil, BIOCONTROL, YIELD, 030104 developmental biology, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, FUNGUS, chemistry, Antagonism, Surfactin, 010606 plant biology & botany
Abstract

Rice monoculture in acid sulfate soils (ASSs) is affected by a wide range of abiotic and biotic constraints, including rice blast caused by Pyricularia oryzae. To progress towards a more sustainable agriculture, our research aimed to screen the biocontrol potential of indigenous Bacillus spp. against blast disease by triggering induced systemic resistance (ISR) via root application and direct antagonism. Strains belonging to the B. altitudinis and B. velezensis group could protect rice against blast disease by ISR. UPLC–MS and marker gene replacement methods were used to detect cyclic lipopeptide (CLiP) production and construct CLiPs deficient mutants of B. velezensis, respectively. Here we show that the CLiPs fengycin and iturin are both needed to elicit ISR against rice blast in potting soil and ASS conditions. The CLiPs surfactin, iturin and fengycin completely suppressed P. oryzae spore germination resulting in disease severity reduction when co-applied on rice leaves. In vitro microscopic assays revealed that iturin and fengycin inhibited the mycelial growth of the fungus P. oryzae, while surfactin had no effect. The capacity of indigenous Bacillus spp. to reduce rice blast by direct and indirect antagonism in ASS conditions provides an opportunity to explore their usage for rice blast control in the field.

Published
2021
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9. Chelator sensing and lipopeptide interplay mediates molecular interspecies interactions between soil bacilli and pseudomonads

Author

E. De Pauw, S. Andric, R. De Mot, Sébastien Steels, A. Rigolet, Marc Ongena, Monica Höfte, Anthony Arguelles Arias, Grégory Hoff, Thibault Meyer, and Andréa McCann

Subjects
Genetics, Bacilli, Rhizosphere, chemistry.chemical_compound, biology, chemistry, Pseudomonas, Metabolome, Lipopeptide, Bacillus, Microbiome, biology.organism_classification, Surfactin
Abstract

Some bacterial species are important members of the rhizosphere microbiome and confer protection to the host plant against pathogens. However, our knowledge of the multitrophic interactions determining the ecological fitness of these biocontrol bacteria in their highly competitive natural niche is still limited. In this work, we investigated the molecular mechanisms underlying interactions between B. velezensis, considered as model plant-associated and beneficial species in the Bacillus genus, and Pseudomonas as a rhizosphere-dwelling competitor. Our data show that B. velezensis boosts its arsenal of specialized antibacterials upon the perception of the secondary siderophore enantio-pyochelin produced by phylogenetically distinct pseudomonads and some other genera. We postulate that B. velezensis has developed some chelator sensing systems to learn about the identity of its surrounding competitors. Illustrating the multifaceted molecular response of Bacillus, surfactin is another crucial component of the secondary metabolome mobilized in interbacteria competition. Its accumulation not only enhances motility but, unexpectedly, the lipopeptide also acts as a chemical trap that reduces the toxicity of other lipopeptides released by Pseudomonas challengers. This in turn favors the persistence of Bacillus populations upon competitive root colonization. Our work thus highlights new ecological roles for bacterial secondary metabolites acting as key drivers of social interactions.

Published
2021
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10. Characterization of the first tetrameric transcription factor of the GntR superfamily with allosteric regulation from the bacterial pathogen Agrobacterium fabrum

Author

Armelle Vigouroux, Anaïs Naretto, Pierre Legrand, Aurélie Di Cicco, Ludovic Vial, Daniel Lévy, Sébastien Renoud, Céline Lavire, Jeanne Doré, Magali Aumont-Nicaise, Solange Moréra, Thibault Meyer, 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), Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Synchroton Soleil, Division Experience/Ligne Nanoscopium, L'Orme des Merisiers, Gif-sur-Yvette, ANR-10-INSB-05-01 INSB ANR-10-INSB-0501, Universite de LyonED341-E2M2French Ministere de l'Education Nationale, de l'Enseignement Superieur et de la RechercheFrench National Research Infrastructure France BioImagingANR10-INBS-04Centre National de la Recherche Scientifique (CNRS)European Commission, Synchrotron SOLEIL (SSOLEIL), Laboratoire Physico-Chimie Curie [Institut Curie] (PCC), Institut Curie [Paris]-Institut de Chimie du CNRS (INC)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Microbiologie et enzymologie structurale (MESB3S), Département Biochimie, Biophysique et Biologie Structurale (B3S), 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), Mesures d'interactions protéine-protéine (PIM), Département Plateforme (PF I2BC), Centre de recherche de l'Institut Curie [Paris], and Institut Curie [Paris]

Subjects
Models, Molecular, Coumaric Acids, Protein Conformation, AcademicSubjects/SCI00010, [SDV]Life Sciences [q-bio], Allosteric regulation, Repressor, Agrobacterium, Biology, Crystallography, X-Ray, Sodium Citrate, 03 medical and health sciences, Allosteric Regulation, Bacterial Proteins, Protein Domains, Transcription (biology), Structural Biology, Genetics, Transcriptional regulation, Genes, Synthetic, Binding site, Promoter Regions, Genetic, Transcription factor, Tetrahydrofolates, 030304 developmental biology, 0303 health sciences, Binding Sites, Effector, 030302 biochemistry & molecular biology, Gene Expression Regulation, Bacterial, DNA binding site, Repressor Proteins, Zinc, Biochemistry, Multigene Family, Protein Multimerization
Abstract

A species-specific region, denoted SpG8-1b allowing hydroxycinnamic acids (HCAs) degradation is important for the transition between the two lifestyles (rhizospheric versus pathogenic) of the plant pathogen Agrobacterium fabrum. Indeed, HCAs can be either used as trophic resources and/or as induced-virulence molecules. The SpG8-1b region is regulated by two transcriptional regulators, namely, HcaR (Atu1422) and Atu1419. In contrast to HcaR, Atu1419 remains so far uncharacterized. The high-resolution crystal structures of two fortuitous citrate complexes, two DNA complexes and the apoform revealed that the tetrameric Atu1419 transcriptional regulator belongs to the VanR group of Pfam PF07729 subfamily of the large GntR superfamily. Until now, GntR regulators were described as dimers. Here, we showed that Atu1419 represses three genes of the HCAs catabolic pathway. We characterized both the effector and DNA binding sites and identified key nucleotides in the target palindrome. From promoter activity measurement using defective gene mutants, structural analysis and gel-shift assays, we propose N5,N10-methylenetetrahydrofolate as the effector molecule, which is not a direct product/substrate of the HCA degradation pathway. The Zn2+ ion present in the effector domain has both a structural and regulatory role. Overall, our work shed light on the allosteric mechanism of transcription employed by this GntR repressor.

Published
2020
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11. Structural basis for two efficient modes of agropinic acid opine import into the bacterial pathogen Agrobacterium tumefaciens

Author

Céline Lavire, Loïc Marty, Yves Dessaux, Thibault Meyer, Armelle Vigouroux, Magali Aumont-Nicaise, Solange Moréra, Franck Pelissier, 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), Microbiologie et enzymologie structurale (MESB3S), Département Biochimie, Biophysique et Biologie Structurale (B3S), 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), Institut de Chimie des Substances Naturelles (ICSN), Institut de Chimie du CNRS (INC)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Intéractions Plantes-Bactéries (PBI), Département Microbiologie (Dpt Microbio), French Ministere de l'Education Nationale, de l'Enseignement Superieur et de la Recherche Centre National de la Recherche Scientifique (CNRS)French National Research Agency (ANR) ANR-12-BSV8-0003-01/02/03FRISBI ANR-10-INSB-05-01I2BC mass spectrometry SICaPS platform, Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay, Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay, Bio-inspired Chemistry and Ecological Innovations (ChimEco), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), and Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL)

Subjects
[SDV]Life Sciences [q-bio], opine, Opine, ATP-binding cassette transporter, Biochemistry, 03 medical and health sciences, chemistry.chemical_compound, Ti plasmid, crystal structures, octopine, periplasmic binding protein, crown-gall, gene, Molecular Biology, Gene, transformed plants, 030304 developmental biology, degradation, Octopine, 0303 health sciences, region, biology, Catabolism, 030302 biochemistry & molecular biology, catabolism, Cell Biology, Agrobacterium tumefaciens, biology.organism_classification, agrobacterium tumefaciens, cyclase, ti-plasmid, chemistry, mannopinic acid, affinity, Bacteria
Abstract

Agrobacterium tumefaciens pathogens genetically modify their host plants to drive the synthesis of opines in plant tumors. The mannityl-opine family encompasses mannopine, mannopinic acid, agropine and agropinic acid. These opines serve as nutrients and are imported into bacteria via periplasmic-binding proteins (PBPs) in association with ABC transporters. Structural and affinity data on agropine and agropinic acid opines bound to PBPs are currently lacking. Here, we investigated the molecular basis of AgtB and AgaA, proposed as the specific PBP for agropine and agropinic acid import, respectively. Using genetic approaches and affinity measurements, we identified AgtB and its transporter as responsible for agropine uptake in agropine-assimilating agrobacteria. Nonetheless, we showed that AgtB binds agropinic acid with a higher affinity than agropine, and we structurally characterized the agropinic acid-binding mode through three crystal structures at 1.4, 1.74 and 1.9 Å resolution. In the crystallization time course, obtaining a crystal structure of AgtB with agropine was unsuccessful due to the spontaneous lactamization of agropine into agropinic acid. AgaA binds agropinic acid only with a similar affinity in nanomolar range as AgtB. The structure of AgaA bound to agropinic acid at 1.65 Å resolution defines a different agropinic acid-binding signature. Our work highlights the structural and functional characteristics of two efficient agropinic acid assimilation pathways, of which one is also involved in agropine assimilation.

Published
2019
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12. Ecological conditions and molecular determinants involved in agrobacterium lifestyle in tumors

Author

Céline Lavire, Clémence Thiour-Mauprivez, Ludovic Vial, Thibault Meyer, Gilles Comte, Florence Wisniewski-Dyé, Isabelle Kerzaon, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), CNRS (Mission pour l'interdisciplinarite, Agromics 2014-2016), French national program EC2CO-Biohefect/Ecodyn/Dril/MicrobiEn (IBAD), and French Ministere de l'Education Nationale, de l'Enseignement Superieur et de la Recherche

Subjects
crown gall, galle du collet, Agrobacterium, [SDV]Life Sciences [q-bio], Virulence, Plant Science, Disease, lcsh:Plant culture, 03 medical and health sciences, plant defense, Plant defense against herbivory, Agrobacterium tumefaciens, tumor lifestyle, molecular traits, competition, Gall, lcsh:SB1-1110, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, Genetics, 0303 health sciences, Rhizosphere, biology, 030306 microbiology, fungi, food and beverages, biology.organism_classification, agrobacterium tumefaciens, bacteria, compétition, Bacteria
Abstract

International audience; The study of pathogenic agents in their natural niches allows for a better understanding of disease persistence and dissemination. Bacteria belonging to the Agrobacterium genus are soil-borne and can colonize the rhizosphere. These bacteria are also well known as phytopathogens as they can cause tumors (crown gall disease) by transferring a DNA region (T-DNA) into a wide range of plants. Most reviews on Agrobacterium are focused on virulence determinants, T-DNA integration, bacterial and plant factors influencing the efficiency of genetic transformation. Recent research papers have focused on the plant tumor environment on the one hand, and genetic traits potentially involved in bacterium-plant interactions on the other hand. The present review gathers current knowledge about the special conditions encountered in the tumor environment along with the Agrobacterium genetic determinants putatively involved in bacterial persistence inside a tumor. By integrating recent metabolomic and transcriptomic studies, we describe how tumors develop and how Agrobacterium can maintain itself in this nutrient-rich but stressful and competitive environment.

Published
2019
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14. The plant defense signal galactinol is specifically used as a nutrient by the bacterial pathogen Agrobacterium fabrum

Author

Céline Lavire, Magali Aumont-Nicaise, Gilles Comte, Solange Moréra, Thibault Meyer, Ludovic Vial, Armelle Vigouroux, Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay, Département Biochimie, Biophysique et Biologie Structurale (B3S), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay, Microbiologie et enzymologie structurale (MESB3S), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay-Institut de Biologie Intégrative de la Cellule (I2BC), Mesures d'interactions protéine-protéine (PIM), Département Plateforme (PF I2BC), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), 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), 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), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), FRISBI ANR-10-INSB-05-01, and Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, Protein Conformation, [SDV]Life Sciences [q-bio], ATP-binding cassette transporter, crystal structure, sugar transport, bacteria, ABC transporter, microbiology, agrobacterium, galactinol, periplasmic binding protein, RFOs, plant defense, Agrobacterium fabrum, Crystallography, X-Ray, Disaccharides, Biochemistry, chemistry.chemical_compound, Plant defense against herbivory, Raffinose, MESB3S, bactérie, Rhizosphere, food and beverages, Plants, Protein Structure and Folding, PF, rhizosphère, B3S, agent pathogène, Agrobacterium, 030106 microbiology, Biology, Stachyose, 03 medical and health sciences, Bacterial Proteins, oligosaccharide, Melibiose, Molecular Biology, fungi, Nutrients, Cell Biology, biology.organism_classification, PIM, chemistry, Agrobacterium tumefaciens, Galactose
Abstract

The bacterial plant pathogen Agrobacterium fabrum uses periplasmic-binding proteins (PBPs) along with ABC transporters to import a wide variety of plant molecules as nutrients. Nonetheless, how A. fabrum acquires plant metabolites is incompletely understood. Using genetic approaches and affinity measurements, we identified here the PBP MelB and its transporter as being responsible for the uptake of the raffinose family of oligosaccharides (RFO), which are the most widespread d-galactose–containing oligosaccharides in higher plants. We also found that the RFO precursor galactinol, recently described as a plant defense molecule, is imported into Agrobacterium via MelB with nanomolar range affinity. Structural analyses and binding mode comparisons of the X-ray structures of MelB in complex with raffinose, stachyose, galactinol, galactose, and melibiose (a raffinose degradation product) revealed how MelB recognizes the nonreducing end galactose common to all these ligands and that MelB has a strong preference for a two-unit sugar ligand. Of note, MelB conferred a competitive advantage to A. fabrum in colonizing the rhizosphere of tomato plants. Our integrative work highlights the structural and functional characteristics of melibiose and galactinol assimilation by A. fabrum, leading to a competitive advantage for these bacteria in the rhizosphere. We propose that the PBP MelB, which is highly conserved among both symbionts and pathogens from Rhizobiace family, is a major trait in these bacteria required for early steps of plant colonization.

Published
2018
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15. Genomic characterization of Ensifer aridi, a proposed new species of nitrogen-fixing rhizobium recovered from Asian, African and American deserts

Author

Céline Lavire, David Chapulliot, Abdelkarim Filali-Maltouf, H. S. Gehlot, Antoine Le Quéré, José-Antonio Munive, Sonam Rathi, Guadalupe Rocha, Marine Rohmer, Nisha Tak, Ilham Sakrouhi, Thibault Meyer, Dany Severac, 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), Laboratoire de Microbiologie et Biologie Moléculaire, Université Mohammed V de Rabat [Agdal], BNF & Microbial Genomics Lab, Department of Botany, Jai Narain Vyas University, Université de Lyon, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), Instituto de Ciencias, Benemérita Universidad Autónoma, Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Project SEP-CONACYT-ANUIES-ECOS NORD France [M08-A02], Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Le Quéré, Antoine, Université Mohammed V de Rabat [Agdal] (UM5), Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-BioCampus (BCM), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), 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 ), Université Mohammed 5 Agdal, Université de Lyon (COMUE), Ecologie microbienne ( EM ), Centre National de la Recherche Scientifique ( CNRS ) -Ecole Nationale Vétérinaire de Lyon ( ENVL ) -Université Claude Bernard Lyon 1 ( UCBL ), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique ( INRA ) -VetAgro Sup ( VAS ), Montpellier GenomiX, and Institut de Génomique Fonctionnelle

Subjects
0301 basic medicine, Biodiversité et Ecologie, bactérie fixatrice d'azote, sinorhizobium, adaptation, comparative genomics, Genome, mexique, rhizobium, maroc, octopine, Desert, Rhizobium-legume symbiosis, Phylogeny, High-Throughput Nucleotide Sequencing, asie, afrique, Genomics, legume, rhizobium-legume symbiosis, analyse phylogeographique, Phenotype, Sinorhizobium, ensifer, desert, Nitrogen fixation, Rhizobium, Desert Climate, Genome, Plant, Research Article, Biotechnology, nopaline, Asia, 030106 microbiology, interaction hôte symbiote, Biology, Synteny, légumineuse, amérique, Evolution, Molecular, Biodiversity and Ecology, 03 medical and health sciences, analyse de génome, Symbiosis, Phylogenetics, Nitrogen Fixation, Botany, Genetics, Adaptation, basicity, Comparative genomics, [ SDE.BE ] Environmental Sciences/Biodiversity and Ecology, Desert climate, désert, Computational Biology, Molecular Sequence Annotation, 15. Life on land, biology.organism_classification, inde, Ensifer, 030104 developmental biology, inositol, Africa, america, profilage génétique, alcalinité, Americas, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Rhizobium- legume symbiosis
Abstract

Background Nitrogen fixing bacteria isolated from hot arid areas in Asia, Africa and America but from diverse leguminous plants have been recently identified as belonging to a possible new species of Ensifer (Sinorhizobium). In this study, 6 strains belonging to this new clade were compared with Ensifer species at the genome-wide level. Their capacities to utilize various carbon sources and to establish a symbiotic interaction with several leguminous plants were examined. Results Draft genomes of selected strains isolated from Morocco (Merzouga desert), Mexico (Baja California) as well as from India (Thar desert) were produced. Genome based species delineation tools demonstrated that they belong to a new species of Ensifer. Comparison of its core genome with those of E. meliloti, E. medicae and E. fredii enabled the identification of a species conserved gene set. Predicted functions of associated proteins and pathway reconstruction revealed notably the presence of transport systems for octopine/nopaline and inositol phosphates. Phenotypic characterization of this new desert rhizobium species showed that it was capable to utilize malonate, to grow at 48 °C or under high pH while NaCl tolerance levels were comparable to other Ensifer species. Analysis of accessory genomes and plasmid profiling demonstrated the presence of large plasmids that varied in size from strain to strain. As symbiotic functions were found in the accessory genomes, the differences in symbiotic interactions between strains may be well related to the difference in plasmid content that could explain the different legumes with which they can develop the symbiosis. Conclusions The genomic analysis performed here confirms that the selected rhizobial strains isolated from desert regions in three continents belong to a new species. As until now only recovered from such harsh environment, we propose to name it Ensifer aridi. The presented genomic data offers a good basis to explore adaptations and functionalities that enable them to adapt to alkalinity, low water potential, salt and high temperature stresses. Finally, given the original phylogeographic distribution and the different hosts with which it can develop a beneficial symbiotic interaction, Ensifer aridi may provide new biotechnological opportunities for degraded land restoration initiatives in the future. Electronic supplementary material The online version of this article (doi:10.1186/s12864-016-3447-y) contains supplementary material, which is available to authorized users.

Published
2017
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16. Essential oils of Origanum compactum and Thymus vulgaris exert a protective effect against the phytopathogen Allorhizobium vitis

Author

Isabelle Kerzaon, Rachid Benkirane, Khaoula Habbadi, Vincent Gaillard, El Hassan Achbani, Céline Lavire, Ludovic Vial, Thibault Meyer, Abdellatif Benbouazza, Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM), Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Vétérinaire de Lyon (ENVL)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Ecole Nationale Vétérinaire de Lyon (ENVL), Institut national de la recherche agronomique [Maroc] (INRA Maroc), Université Ibn Tofail [Kenitra], Partenaires INRAE, project 'Biological control of Agrobacterium vitis, the causal agent of Crown gall on grapevines' PRAD 14-08, regional center of the National Institute for Agricultural Research Meknes (INRA), and French national programme EC2CO-Biohefect/Ecodyn//Dril/MicrobiEn (IBAD)

Subjects
0106 biological sciences, 0301 basic medicine, Agrobacterium, Health, Toxicology and Mutagenesis, [SDV]Life Sciences [q-bio], 030106 microbiology, Thymus vulgaris, Biological pest control, Microbial Sensitivity Tests, 01 natural sciences, Thymus Plant, Origanum compactum, 03 medical and health sciences, chemistry.chemical_compound, Rhizobiaceae, Origanum, Oils, Volatile, Plant Oils, Environmental Chemistry, Gall, Vitis, Carvacrol, Allorhizobium vitis, Thymol, Plant Diseases, 2. Zero hunger, biology, Traditional medicine, Inoculation, food and beverages, Biocontrol, General Medicine, biology.organism_classification, Pollution, Anti-Bacterial Agents, Crown gall, chemistry, Essential oils, Monoterpenes, Cymenes, Bacteria, 010606 plant biology & botany
Abstract

International audience; Allorhizobium (Agrobacterium) vitis is a host-specific pathogenic bacterium that causes grapevine crown gall disease, affecting vine growth and production worldwide. The antibacterial activities of different aromatic plant essential oils were tested in vitro and in planta against A. vitis. Among the essential oils tested, those of Origanum compactum and Thymus vulgaris showed the most significant in vitro antibacterial activities, with a MIC of 0.156 and 0.312 mg/mL, respectively. A synergistic effect of these two essential oils (1:1) was observed and confirmed by the checkerboard test. Carvacrol (61.8%) and thymol (47.8%) are, respectively, the major compounds in the essential oils of O. compactum and T. vulgaris and they have been shown to be largely responsible for the antibacterial activities of their corresponding essential oils. Results obtained in vitro were reinforced by an in planta pathogenicity test. A mixture of O. compactum and T. vulgaris essential oils (1:1), inoculated into the injured stem of a tomato plant and a grapevine at 0.312 mg/mL as a preventive treatment, reduced both the number of plants developing gall symptoms and the size of the tumors.

Published
2017
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