Moubset Oumaima, Filloux Denis, Fontes Hugo, Julian Charlotte, Fernandez Emmanuel, Galzi Serge, Blondin Laurence, Chehida Sélim Ben, Lett Jean-Michel, Mesléard François, Kraberger Simona, Custer Joy M, Salywon Andrew, Makings Elizabeth, Marais Armelle, Chiroleu Frédéric, Lefeuvre Pierre, Martin Darren P, Candresse Thierry, Varsani Arvind, Ravigné Virginie, Roumagnac Philippe
UMR PHIM, CIRAD, Baillarguet TA A-54/K, Montpellier 34090, France.
PHIM Plant Health Institute, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Baillarguet TA A-54/K, Montpellier 34090, France.
Virus Evol. 2024 Mar 9;10(1):veae025. doi: 10.1093/ve/veae025. eCollection 2024.
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 (), 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 in France were not associated with a lower PAV prevalence or richness than native populations of 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 family) and one putatively horizontally transmitted phytovirus (belonging to the family) were identified from plants in the introduced area. Collectively, these characteristics of the -associated PAV community in southern France suggest that a virome release phase may have immediately followed the introduction of 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.
人类介导的植物物种向新区域引入的增加，导致了外来入侵植物物种（IEPS）的增多，这对生物多样性和生态系统过程产生了重大影响。一种普遍接受的入侵机制是由天敌释放假说（ERH）提出的，该假说认为，在新环境中摆脱了本土食草动物和天敌的IEPS能够胜过本土物种并成为入侵物种。我们在此提出病毒组释放假说（VRH），作为传统ERH以病毒为中心的变体，传统ERH仅关注天敌。VRH预测，在IEPS传播过程中，垂直传播的植物相关病毒（PAV，包括植物病毒和真菌病毒）应会一同被引入，而IEPS的水平传播PAV由于当地媒介的不适应，应会被留在原地或在引入地区无法进行本地传播。为了验证VRH，我们比较了本土植物物种与一种入侵性禾本科植物——甘蔗须芒草（）在其引入范围（法国南部）和一个原生范围地区（美国亚利桑那州索诺兰沙漠）的病毒组丰富度和组成，以及PAV的流行情况、共感染情况、宿主范围和传播模式。与VRH相反，我们发现法国的甘蔗须芒草入侵种群与来自美国的本土种群相比，PAV流行率或丰富度并不低。然而，病毒组组成的比较和网络分析进一步揭示，法国生态系统中植物 - 病毒的相互作用更加多样和复杂，真菌病毒丰富度显著。除真菌病毒外，在引入地区的甘蔗须芒草植物中仅鉴定出一种可能垂直传播的植物病毒（属于 科）和一种可能水平传播的植物病毒（属于 科）。总体而言，法国南部与甘蔗须芒草相关的PAV群落的这些特征表明，在20世纪60年代或70年代甘蔗须芒草被引入法国后，可能紧接着进入了一个病毒组释放阶段，从那时起，这种IEPS的入侵种群已经从这个病毒组释放阶段过渡出来，并开始与几种当地真菌病毒和一些当地植物病毒相互作用。
