Virome release of an invasive exotic plant species in southern France

Moubset Oumaima, Filloux Denis, Fontes Hugo, Julian Charlotte, Fernandez Emmanuel, Galzi Serge, Blondin Laurence, Ben Chehida Sélim, Lett Jean-Michel, Mesleard François, Kraberger Simona, Custer Joy M., Salywon Andrew M., Makings Elizabeth, Marais Armelle, Chiroleu Frédéric, Lefeuvre Pierre, Martin Darren Patrick, Candresse Thierry, Varsani Arvind, Ravigné Virginie, Roumagnac Philippe. 2024. Virome release of an invasive exotic plant species in southern France. Virus Evolution, 10 (1):veae025, 16 p.

Url - jeu de données - Entrepôt autre : https://doi.org/10.5281/zenodo.10159099

Résumé : The increase in human-mediated introduction of plant species to new regions has resulted in a rise of invasive exotic plant species (IEPS) that has had significant effects on biodiversity and ecosystem processes. One commonly accepted mechanism of invasions is that proposed by the enemy release hypothesis (ERH), which states that IEPS free from their native herbivores and natural enemies in new environments can outcompete indigenous species and become invasive. We here propose the virome release hypothesis (VRH) as a virus-centered variant of the conventional ERH that is only focused on enemies. The VRH predicts that vertically transmitted plant-associated viruses (PAV, encompassing phytoviruses and mycoviruses) should be co-introduced during the dissemination of the IEPS, while horizontally transmitted PAV of IEPS should be left behind or should not be locally transmitted in the introduced area due to a maladaptation of local vectors. To document the VRH, virome richness and composition as well as PAV prevalence, co-infection, host range, and transmission modes were compared between indigenous plant species and an invasive grass, cane bluestem (Bothriochloa barbinodis), in both its introduced range (southern France) and one area of its native range (Sonoran Desert, Arizona, USA). Contrary to the VRH, we show that invasive populations of B. barbinodis in France were not associated with a lower PAV prevalence or richness than native populations of B. barbinodis from the USA. However, comparison of virome compositions and network analyses further revealed more diverse and complex plant–virus interactions in the French ecosystem, with a significant richness of mycoviruses. Setting mycoviruses apart, only one putatively vertically transmitted phytovirus (belonging to the Amalgaviridae family) and one putatively horizontally transmitted phytovirus (belonging to the Geminiviridae family) were identified from B. barbinodis plants in the introduced area. Collectively, these characteristics of the B. barbinodis-associated PAV community in southern France suggest that a virome release phase may have immediately followed the introduction of B. barbinodis to France in the 1960s or 1970s, and that, since then, the invasive populations of this IEPS have already transitioned out of this virome release phase, and have started interacting with several local mycoviruses and a few local plant viruses.

Mots-clés Agrovoc : virus des végétaux, Geminiviridae, espèce envahissante, Bothriochloa, introduction de plantes, vecteur de maladie, transmission des maladies, taxonomie, identification

Mots-clés géographiques Agrovoc : France

Mots-clés complémentaires : Bothriochloa barbinodis

Mots-clés libres : Viral ecology, Viral metagenomics, Plant-associated viruses, Invasive exotic plant species

Classification Agris : H20 - Maladies des plantes
F40 - Écologie végétale

Champ stratégique Cirad : CTS 4 (2019-) - Santé des plantes, des animaux et des écosystèmes

Agences de financement européennes : European Regional Development Fund

Agences de financement hors UE : Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Agence Nationale de la Recherche, Conseil Régional de La Réunion

Projets sur financement : (FRA) Mesure et cartographie de la richesse des virus des plante à l'échelle de l'écosytème

Auteurs et affiliations

• Moubset Oumaima, CIRAD-BIOS-UMR PHIM (FRA)
• Filloux Denis, CIRAD-BIOS-UMR PHIM (FRA)
• Fontes Hugo, La Tour du Valat, Centre de recherche pour la conservation des zones humides méditerranéennes (FRA)
• Julian Charlotte, CIRAD-BIOS-UMR PHIM (FRA)
• Fernandez Emmanuel, CIRAD-BIOS-UMR PHIM (FRA)
• Galzi Serge, CIRAD-BIOS-UMR PHIM (FRA)
• Blondin Laurence, CIRAD-BIOS-UMR PHIM (FRA)
• Ben Chehida Sélim, CIRAD-BIOS-UMR PVBMT (REU)
• Lett Jean-Michel, CIRAD-BIOS-UMR PVBMT (REU)
• Mesleard François, La Tour du Valat, Centre de recherche pour la conservation des zones humides méditerranéennes (FRA)
• Kraberger Simona, Arizona State University (USA)
• Custer Joy M., Arizona State University (USA)
• Salywon Andrew M., Desert Botanical Garden (USA)
• Makings Elizabeth, Arizona State University (USA)
• Marais Armelle, INRAE (FRA)
• Chiroleu Frédéric, CIRAD-BIOS-UMR PVBMT (REU) ORCID: 0000-0002-4874-5357
• Lefeuvre Pierre, CIRAD-BIOS-UMR PVBMT (REU)
• Martin Darren Patrick, Institute of Infectious Diseases and Molecular Medicine (ZAF)
• Candresse Thierry, INRAE (FRA)
• Varsani Arvind, Arizona State University (USA)
• Ravigné Virginie, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0002-4252-2574
• Roumagnac Philippe, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0001-5002-6039 - auteur correspondant

Source : Cirad-Agritrop (https://agritrop.cirad.fr/609129/)

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