Virome release of an invasive exotic plant species in southern France
Oumaima Moubset
(1, 2)
,
Denis Filloux
(1)
,
Hugo Fontes
(3, 4)
,
Charlotte Julian
(1)
,
Emmanuel Fernandez
(1)
,
Serge Galzi
(1, 2)
,
Laurence Blondin
(1)
,
Sélim Ben Chehida
(5)
,
Jean-Michel Lett
(5, 2)
,
François Mesléard
(3, 4)
,
Simona Kraberger
(6)
,
Joy M Custer
(6)
,
Andrew Salywon
(7)
,
Elizabeth Makings
(6)
,
Armelle Marais
(8)
,
Frédéric Chiroleu
(5)
,
Pierre Lefeuvre
(5, 9)
,
Darren P Martin
(10)
,
Thierry Candresse
(8)
,
Arvind Varsani
(6, 10)
,
Virginie Ravigné
(1)
,
Philippe Roumagnac
(1)
1
UMR PHIM -
Plant Health Institute of Montpellier
2 Cirad-BIOS - Département Systèmes Biologiques
3 IMBE - Institut méditerranéen de biodiversité et d'écologie marine et continentale
4 Institut de recherche de la Tour du Valat
5 UMR PVBMT - Peuplements végétaux et bioagresseurs en milieu tropical
6 ASU - Arizona State University [Tempe]
7 Desert Botanical Garden
8 BFP - Biologie du fruit et pathologie
9 CERAMATHS - Laboratoire de Matériaux Céramiques et de Mathématiques
10 University of Cape Town
2 Cirad-BIOS - Département Systèmes Biologiques
3 IMBE - Institut méditerranéen de biodiversité et d'écologie marine et continentale
4 Institut de recherche de la Tour du Valat
5 UMR PVBMT - Peuplements végétaux et bioagresseurs en milieu tropical
6 ASU - Arizona State University [Tempe]
7 Desert Botanical Garden
8 BFP - Biologie du fruit et pathologie
9 CERAMATHS - Laboratoire de Matériaux Céramiques et de Mathématiques
10 University of Cape Town
Hugo Fontes
- Fonction : Auteur
- PersonId : 1378969
- ORCID : 0000-0002-7826-6680
Serge Galzi
- Fonction : Auteur
Jean-Michel Lett
- Fonction : Auteur
- PersonId : 1153049
- ORCID : 0000-0003-2013-0016
Armelle Marais
- Fonction : Auteur
- PersonId : 740106
- IdHAL : armelle-marais
- ORCID : 0000-0003-2482-1543
- IdRef : 25311957X
Frédéric Chiroleu
- Fonction : Auteur
- PersonId : 867044
- ORCID : 0000-0002-4874-5357
- IdRef : 228346762
Pierre Lefeuvre
- Fonction : Auteur
- PersonId : 802635
- ORCID : 0000-0003-2645-8098
Darren P Martin
- Fonction : Auteur
- PersonId : 1262734
- ORCID : 0000-0002-8785-0870
Thierry Candresse
- Fonction : Auteur
- PersonId : 741063
- IdHAL : thierry-candresse
- ORCID : 0000-0001-9757-1835
- IdRef : 058616438
Arvind Varsani
- Fonction : Auteur
- PersonId : 765062
- ORCID : 0000-0003-4111-2415
Virginie Ravigné
- Fonction : Auteur
- PersonId : 1136571
- ORCID : 0000-0002-4252-2574
- IdRef : 07925442X
Philippe Roumagnac
- Fonction : Auteur
- PersonId : 802733
- ORCID : 0000-0001-5002-6039
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.
Format du dépôt | Fichier |
---|---|
Type de dépôt | Article dans une revue |
Titre |
en
Virome release of an invasive exotic plant species in southern France
|
Résumé |
en
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.
|
Auteur(s) |
Oumaima Moubset
1, 2
, Denis Filloux
1
, Hugo Fontes
3, 4
, Charlotte Julian
1
, Emmanuel Fernandez
1
, Serge Galzi
1, 2
, Laurence Blondin
1
, Sélim Ben Chehida
5
, Jean-Michel Lett
5, 2
, François Mesléard
3, 4
, Simona Kraberger
6
, Joy M Custer
6
, Andrew Salywon
7
, Elizabeth Makings
6
, Armelle Marais
8
, Frédéric Chiroleu
5
, Pierre Lefeuvre
5, 9
, Darren P Martin
10
, Thierry Candresse
8
, Arvind Varsani
6, 10
, Virginie Ravigné
1
, Philippe Roumagnac
1
1
UMR PHIM -
Plant Health Institute of Montpellier
( 1100829 )
- CIRAD Campus International de Baillarguet TA A-54/K
34398 Montpellier
- France
2
Cirad-BIOS -
Département Systèmes Biologiques
( 168219 )
- Avenue Agropolis TA A-DIR / 04 34398 Montpellier Cedex 5 France
- France
3
IMBE -
Institut méditerranéen de biodiversité et d'écologie marine et continentale
( 188653 )
- Aix Marseille Université, Campus Etoile, Faculté St-Jérôme case 421 Av. . escadrille Normandie-Niemen 13397 MARSEILLE CEDEX 20
- France
4
Institut de recherche de la Tour du Valat
( 522913 )
- Tour du Valat Le Sambuc - 13200 Arles - France Fondation 301233
- France
5
UMR PVBMT -
Peuplements végétaux et bioagresseurs en milieu tropical
( 1001933 )
- Faculté des Sciences et techniques - Université de La Réunion 15 avenue René Cassin CS92003 97744 Saint-Denis Cédex 9 pour le Cirad Station de Ligne-Paradis - 7 chemin de l'IRAT - 97410 Saint-Pierre
- La Réunion
6
ASU -
Arizona State University [Tempe]
( 251827 )
- 325 E Apache Blvd, Tempe, AZ 85281, États-Unis
- États-Unis
7
Desert Botanical Garden
( 492323 )
- 1201 N. Galvin Parkway
Phoenix, AZ 85008
- États-Unis
8
BFP -
Biologie du fruit et pathologie
( 1002364 )
- Centre INRAE Bordeaux-Aquitaine 71 avenue Bourlaux BP81 F-33883 Villenave d'Ornon
- France
9
CERAMATHS -
Laboratoire de Matériaux Céramiques et de Mathématiques
( 1077390 )
- Campus Le Mont Houy 59313 Valenciennes Cedex 9
- France
10
University of Cape Town
( 303907 )
- Private Bag X3, Rondebosch 7701, South Africa
- Afrique du Sud
|
Vulgarisation |
Non
|
Comité de lecture |
Oui
|
Audience |
Internationale
|
Langue du document |
Anglais
|
Licence |
Paternité - Pas d'utilisation commerciale
|
Nom de la revue |
|
Public visé |
Scientifique
|
Date de publication |
2024-03-09
|
Volume |
10
|
Numéro |
1
|
Page/Identifiant |
veae025
|
Domaine(s) |
|
Données associées | |
Projet(s) ANR |
|
Financement |
|
Mots-clés |
en
viral ecology, viral metagenomics, plant-associated viruses, invasive exotic plant species
|
DOI | 10.1093/ve/veae025 |
UT key WOS | 001195230500001 |
Origine :
Fichiers éditeurs autorisés sur une archive ouverte
Licence : Paternité - Pas d'utilisation commerciale - CC BY 4.0
Licence : Paternité - Pas d'utilisation commerciale - CC BY 4.0
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