The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99-108

Samuel Roberts Noble Foundation, Plant Biology Division, Ardmore, Oklahoma 73401, USA.
Nature Reviews Microbiology (Impact Factor: 23.57). 02/2011; 9(2):99-108. DOI: 10.1038/nrmicro2491
Source: PubMed


Although viruses are most often studied as pathogens, many are beneficial to their hosts, providing essential functions in some cases and conditionally beneficial functions in others. Beneficial viruses have been discovered in many different hosts, including bacteria, insects, plants, fungi and animals. How these beneficial interactions evolve is still a mystery in many cases but, as discussed in this Review, the mechanisms of these interactions are beginning to be understood in more detail.

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    • "Studies of plant–virus interactions in wild ecosystems are still limited (Cooper & Jones, 2006; Alexander et al., 2014; Roossinck & Garc ıa-Arenal, 2015) and although there are well documented examples of viruses causing obvious diseases in wild plants, affecting plant population sizes and plant ecosystem composition (Malmstrom et al., 2005; Power et al., 2011; R ua et al., 2011; Rodelo-Urrego et al., 2013; Prendeville et al., 2014), most virus infections in wild plants are asymptomatic (Pag an et al., 2010; Prendeville et al., 2012; Roossinck, 2012; Stobbe & Roossinck, 2014). Indeed, it has been proposed that plant viruses would most often be commensals, or even mutualists of plants, and that pathogenic virus infections may be, at least in part, a result of the specific conditions of agricultural ecosystems (Gibbs, 1980; Wren et al., 2006; Xu et al., 2008; Roossinck, 2011). Thus, the pathogenicity of viruses for plants is an ongoing subject of debate, and it is important to understand under which conditions viruses will be virulent parasites of plants. "
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    ABSTRACT: It has been hypothesized that plant-virus interactions vary between antagonism and conditional mutualism according to environmental conditions. This hypothesis is based on scant experimental evidence, and to test it we examined the effect of abiotic factors on the Arabidopsis thaliana-Cucumber mosaic virus (CMV) interaction. Four Arabidopsis genotypes clustering into two allometric groups were grown under six environments defined by three temperature and two light-intensity conditions. Plants were either CMV-infected or mock-inoculated, and the effects of environment and infection on temporal and resource allocation life-history traits were quantified. Life-history traits significantly differed between allometric groups over all environments, with group 1 plants tolerating abiotic stress better than those of group 2. The effect of CMV infection on host fitness (virulence) differed between genotypes, being lower in group 1 genotypes. Tolerance to abiotic stress and to infection was similarly achieved through life-history trait responses, which resulted in resource reallocation from growth to reproduction. Effects of infection varied according to plant genotype and environment from detrimental to beneficial for host fitness. These results are highly relevant and demonstrate that plant viruses can be pleiotropic parasites along the antagonism-mutualism continuum, which should be considered in analyses of the evolution of plant-virus interactions.
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    • "Insect borne plant viruses are a major threat to agricultural systems world-wide, and these associations act in complex ways with climate to affect disease emergence and food production (Parry et al. 2004). Although many viruses are pathogens, negatively affecting the survival, reproduction and distribution of their hosts, many cause no detectable symptoms or even benefit their hosts (Roossinck 2011). Many non-pathogenic virus sequences have been detected from plant tissues (Roossinck 2005), with recent evidence that some plant viruses increase the tolerance of their hosts to elevated environmental stressors including thermal stress (M arquez et al. 2007; Rouhier & Jacquot 2008) and drought (Xu et al. 2008). "

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    • "This observation is consistent with the hypothesis that disease is an evolutionarily disadvantageous state for both viruses and their hosts and generally only occurs as a result of maladapted interactions within newly formed parasitic relationships (Bao and Roossinck 2013). Beyond disease and parasitism, metagenomics may reveal a multitude of mutualistic relationships between viruses and plants (Roossinck 2011, 2013). Metagenomic-oriented approaches are ideally suited to test such hypotheses. "
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    ABSTRACT: In recent years plant viruses have been detected from many environments, including domestic and wild plants and interfaces between these systems-aquatic sources, feces of various animals, and insects. A variety of methods have been employed to study plant virus biodiversity, including enrichment for virus-like particles or virus-specific RNA or DNA, or the extraction of total nucleic acids, followed by next-generation deep sequencing and bioinformatic analyses. All of the methods have some shortcomings, but taken together these studies reveal our surprising lack of knowledge about plant viruses and point to the need for more comprehensive studies. In addition, many new viruses have been discovered, with most virus infections in wild plants appearing asymptomatic, suggesting that virus disease may be a byproduct of domestication. For plant pathologists these studies are providing useful tools to detect viruses, and perhaps to predict future problems that could threaten cultivated plants.
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