Viruses are obligate symbionts that tightly interact with their hosts to complete their life cycle. Each infected cell is confronted with the accumulation of viral products and activities that have evolved to support the replication and spread of the virus in the context of host cell functions and defense responses. Tobacco mosaic virus encodes replicase proteins and coat protein, to replicate and protect the RNA genome, and a movement protein (MP) that binds viral RNA and manipulates the size exclusion limit of plasmodesmata to facilitate the spread of the viral genomic RNA (vRNA). The MP and replicase also interfere with the cellular RNA silencing machinery that influences plant gene expression and development. Moreover, virus-infected cells stimulate the production of a systemic signal ahead of the virus front that triggers genomic recombination leading to heritable genetic changes. Thus viruses can interact with their hosts through diverse molecular interactions. Given the high mutation rate of viruses, these interactions have implications for evolutionary processes and adaptations at the virus-host interface that may contribute to eukaryotic evolution.
Although viruses represent the most abundant biological entity on our planet,1 little is known about their role in eukaryotic evolution. Traditionally, viruses are viewed as selfish parasites that, due to their short generation times and error-prone replication, are able to establish large population diversities that as a swarm of mutant genotypes2 can easily adapt to changes in their host environment. This view about viruses is not surprising given that viruses play a prominent role as pathogens. However, although this perception created the widely held belief that viruses are harmful to their hosts, most viruses may rather be commensals or even be mutualists (e.g., Ref. 3). The biased view that viruses are harmful also applies to plant viruses. Plant viruses are usually seen as pathogens that are studied for the benefit of agriculture. As a consequence, research on plant viruses is usually conducted with the aim of understanding the interactions with economically important and symptomatic hosts and restricted to cultivated laboratory model or monocultured crop species in combination with standard, laboratory-strain, phenotypeproducing viruses. Unfortunately, there is only little information about interactions of viruses with plants in the wild, which creates a huge gap in our overall understanding of viral diversity, evolution, and ecology in natural settings.4 Indeed, given their biodiversity and abundance, viruses likely play an underestimated role in our ecosystems. In reality, any field plant may be commonly infected by one or more viruses. Some known cases of co-infecting viruses that have been addressed experimentally provided insight into the interactions and evolution of plant viruses in association with their hosts.
Thus, if several virus species coexist in one host, they either compete or cooperate. Competition may occur if the infecting virus species compete for important host factors or if the viruses share sequence similarity. The latter has potential to lead to host-mediated exclusion through silencing in which siRNAs derived from infection by the first infecting virus degrade the genome of the second infecting virus. Thus, infection with a mild strain of a virus can “cross-protect” plants against a later infection by a virulent strain of the same virus.6 Cooperation of viruses in mixed infections results if the viruses undergo symbiosis, thus share genetic information or gene products. When this interaction is mutualistic and in balance, the viral species may coevolve and increase fitness together. The interaction can also be parasitic and, thus, leading to an increase in fitness of one viral species at the expense of the other. In the extreme case of symbiosis, one virus is totally dependent on the other, and thus is an obligate symbiont. Facultative or obligate symbiotic relationships between viruses may be favorable through synergy in which one virus supports the virulence of the other virus, for example, through provision of a strong silencing suppressor.7 Importantly, irrespective of the type of symbiosis that has evolved, the underlying tight interactions between co-infecting viruses and between viruses and their hosts are manifestations of specific and highly specialized molecular interactions between viral and cellular proteins and nucleic acids. Given the intimacy of the interactions, viruses could potentially be prime drivers of evolutionary change.4 In fact, the high mutation rate of viruses may continuously provide new protein and nucleic acid variants with potential capacity to drive the further evolution of the corresponding cellular protein and nucleic acid counterparts. With respect to the plant:pathogen interaction, such molecular coevolution contributes to specialization of viruses and hosts and thus may contribute to host associations observed in nature.8 Recent research on the interaction of plant viruses with their hosts has revealed some striking new details about molecular interactions at the host:virus interface, which may act as a yet unexplored creator of novel evolutionary patterns. Here, examples of such interactions, with emphasis on interactions of the plant cell with the tobamovirus tobacco mosaic virus (TMV), are described. Viruses are proposed to have played an important role in various evolutionary scenarios, including the origin of DNA and mammals.9,10 They may continue to act as potent drivers in evolutive processes at the small scale,that is, at molecular interfaces with interacting host proteins and nucleic acids.
Possibility of Evolutive Processes at Molecular Plant: Virus Interfaces Associated with Plant Defense and Viral Counter-Defense
Interaction of Viral Silencing Suppressors with their Cellular Targets
RNA silencing in plants is viewed as a major mechanism to “combat” virus infections.11 In this pathway, viral siRNAs (viRNA) produced from viral dsRNA replication intermediates and intramolecular dsRNA hairpins interact with AGO-containing RISC effector complexes and direct cleavage of homologous viral RNA.12 In response to the evolvement of antiviral silencing, viruses have evolved proteins that suppress the degradation of viral RNA by interfering with RNA silencing at various steps. More than 35 individual silencing suppressor families have been identified from virtually all plant virus types, which indicates the importance and widespread existence of this counterstrategy.
Silencing suppressors are strikingly diverse within and across kingdoms and are often encoded by novel, out-of frame overlapping genes contained within more ancient genes. Although their acquisition appears to be recent and to have evolved independently, suppressors can share analogous biochemical properties. This convergent evolution may have been directed by evolutionary constraints given by the host environment and the molecular interactions within the ecological niche. The activity of silencing suppressors usually depends on direct binding interactions with RNA silencing pathway molecules. It appears likely that the interacting suppressor and its specific target are under constant co-evolution since the interaction places selective pressure on the plant to produce silencing pathway components that no longer serve as target for the viral silencing suppressor and thus to increase antiviral resistance, whereas the virus will respond with the selection of compensatory mutations in suppressor variants that restore this interaction. Thus, virus infection may continuously drive the microevolution of plant proteins at this plant:virus interface.
Evolution Toward “Balanced” Virus: Host Relationships?
The occurrence of mutations at the interface between viral silencing suppressors and their targets may be supported by the existence of virus variants that differ from wildtype virus by causing only mild or attenuated disease symptoms in infected plants. Recent research on natural and artificial severe and mild tobamovirus strains has shown that their attenuation correlated with mutations in the viral silencing suppressor.14–18 The tobamoviral silencing suppressing activity resides in the viral replicase and appears to interfere with siRNA and miRNA methylation18 and, thus, with sRNA stability.19 The mutations in the suppressor function of naturally occurring tobamoviral strains might have been originally selected to complement mutations in the interacting silencing effector target in the natural host. These mutations might in turn have been initially selected to circumvent the activity of the viral suppressor and thus to increase resistance against the virus. Conceivably, the mutations in the silencing suppressor could also have been autonomously selected by the virus in an attempt to weaken the effects of infection on plant host development and thus to maintain host fitness. In this latter scenario, attenuated virus strains may thus evolve in response to selective pressure towards balanced plant:virus interactions that are optimized to maintain the reproductive fitness of both the virus and its host. To gain a realistic view about the evolution of symptomatic versus asymptomatic plant:virus interactions, efforts to identify and to study virus interactions with plants grown in the wild are needed.