Spread of introduced viruses to new plants in natural ecosystems and the threat this poses to plant biodiversity.

Abstract

Biodiversity is endangered in many regions of the world, with loss of native plant species a growing concern requiring a major focus on conservation measures. However, the threat posed by introduced viral pathogens to native plant biodiversity has been ignored almost completely. What occurs when weed seeds and vegetative propagules or seeds of cultivated plants unknowingly infected with viruses are introduced to other regions of the world and the viruses introduced with them then invade indigenous plants for the first time? To what extent are introduced viruses capable of causing damaging diseases which then threaten native plant communities and their species biodiversity, and in what ways can they do this? What can be done about it? In this Opinion piece, our intent is to answer these questions by awakening worldwide interest to undertake research activities that provide a comprehensive understanding of the threat posed by introduced viruses to natural plant ecosystems and biodiversity. Development of such an understanding requires research activities capable of providing in-depth information at both biological and molecular levels. Without such knowledge, effective solutions are unlikely to emerge. New encounters involving viruses and plant species are becoming increasingly common at the agro-ecological interface between managed and natural vegetation. This is because of rapidly increasing human activity, such as agricultural extensification, diversification and intensification practices to increase food production and to address food insecurity, encroaching urbanization and ever increasing international trade in plants and plant products (e.g. Alexander et al., 2014; Jones, 2009, 2014; Roossinck and Garcia-Arenal, 2015). Moreover, inadvertent introduction of new, more efficient virus vectors often exacerbates spread of viruses to previously uninvaded plant species at vegetation interfaces. In the future, the frequency of new encounters between viruses and plant species is likely to increase even more rapidly because of the major alterations in cultivated plant distributions anticipated from climate change (Jones and Barbetti, 2012). Genomic divergence is roughly proportional to the evolutionary distance from a common ancestor, and a high degree of nucleotide sequence diversity over a small geographical range is typical of viruses that have co-evolved locally with native plants (e.g. Coutts et al., 2011; Webster et al., 2007). These viruses are referred to as ‘indigenous’ to distinguish them from others that have arrived from elsewhere and therefore show much less sequence diversity, for which the term ‘introduced’ is used (e.g. Coutts et al., 2011; Jones, 2009; Webster et al., 2007). The threat posed by introduced fungal pathogens to native plant communities and their biodiversity has received considerable attention (e.g. Burdon et al., 2006), and the consequences of virus infection seem likely to resemble those of fungi, including a reduced ability of infected plants to compete with other plants and produce sufficient seed for the next generation (e.g. Cooper and Jones, 2006). However, the threat posed by introduced viral pathogens has received much less attention (Vincent et al., 2014). This is so despite the considerable research activity aimed at understanding how emerging viruses spread in the opposite direction, i.e. from native plants to damage introduced cultivated plant species, especially in the tropics. Such studies normally involve investigation of new encounter scenarios at the agro-ecological interface (e.g. Alexander et al., 2014; Jones, 2009; Roossinck and Garcia-Arenal, 2015). Native plants do not grow as stands of genetically identical plants of the same species exhibiting uniform virus susceptibilities, but as mixed species communities exhibiting both withinand between-species diversity. Natural control measures which serve to decrease virus spread in undisturbed native plant communities, such as mixture with non-hosts, isolation, host resistance/tolerance and the presence of predators and parasites of their vectors, tend to be disrupted when such communities are disturbed,as occurs at the agro-ecological interface and in otherwise disturbed natural vegetation (e.g. Cooper and Jones, 2006; Jones 2009). Co-evolution of viruses with their plant hosts and vectors is thought to have been underway since plants first appeared (Fraile and Garcia-Arenal, 2010; Lovisolo et al., 2003). Thus, long before plants were first domesticated by former hunter gatherers when agriculture began 10 000–15 000 years ago, plants were co-evolving with native plants growing in different world regions. This co-evolutionary process moulded both viruses and native plants (e.g. Vincent et al., 2014). In undisturbed native plant *Correspondence: Email: roger.jones@uwa.edu.au bs_bs_banner