Plant viruses face many challenges in agricultural environments. Although crop fields appear to be abundant resources for these pathogens, it may be difficult for viruses to "escape" from crop environments prior to host senescence or harvesting. One way for viruses to increase the odds of persisting outside of agricultural fields across seasons is by evolving traits that increase transmission opportunities between crops and wild plant communities. There is accumulating evidence that some viruses can achieve this by manipulating crop plant phenotypes in ways that enhance transmission by vectors. Putative manipulations occur through alteration of plant cues (color, size, texture, foliar volatiles, in-leaf metabolites, defenses, and leaf cuticles) that mediate vector orientation, feeding, and dispersal behaviors. Virus effects on host phenotypes are not uniform but appear to exhibit convergence depending on virus traits underlying transmission, particularly the duration of probing and feeding required to acquire and inoculate distinct types of plant viruses. This shared congruence in manipulation strategies and mechanisms across divergent virus lineages suggests that such effects may be adaptive. To discern if this is the case, researchers must consider molecular and environmental constraints on virus evolution, including those imposed by insect vectors from organismal to landscape scales. In this review, we synthesize applied research on vector-borne virus transmission in laboratory and field settings to identify the main factors determining transmission opportunities for plant viruses, and thus, selection pressure to evolve manipulative traits. We then examine these outputs in the context of studies reporting putative instances of plant virus manipulation. Our synthesis reveals important disconnects between virus manipulation studies and actual selection pressures imposed by vectors in real-world contexts.

Plant virus infection fundamentally alters chemical and behavioral phenotypes of hosts and vectors. These alterations often enhance virus transmission, leading researchers to surmise that such effects are manipulations caused by virus adaptations and not just by-products of pathology. But identification of the virus components behind manipulation is missing from most studies performed to date. Here, we evaluate causative empirical evidence that virus components are the drivers of manipulated host and vector phenotypes. To do so, we link findings and methodologies on virus pathology with observational and functional genomics studies on virus manipulation. Our synthesis provides an overview of progress, areas of synergy, and new approaches that will lead to an improved mechanistic understanding of host and vector manipulation by plant viruses.

Plant viruses possess adaptations for facilitating acquisition, retention, and inoculation by vectors. Until recently, it was hypothesized that these adaptations are limited to virus proteins that enable virions to bind to vector mouthparts or invade their internal tissues. However, increasing evidence suggests that viruses can also manipulate host plant phenotypes and vector behaviors in ways that enhance their own transmission. Manipulation of vector-host interactions occurs through virus effects on host cues that mediate vector orientation, feeding, and dispersal behaviors, and thereby, the probability of virus transmission. Effects on host phenotypes vary by pathosystem but show a remarkable degree of convergence among unrelated viruses whose transmission is favored by the same vector behaviors. Convergence based on transmission mechanism, rather than phylogeny, supports the hypothesis that virus effects are adaptive and not just by-products of infection. Based on this, it has been proposed that viruses manipulate hosts through multifunctional proteins that facilitate exploitation of host resources and elicitation of specific changes in host phenotypes. But this proposition is rarely discussed in the context of the numerous constraints on virus evolution imposed by molecular and environmental factors, which figure prominently in research on virus-host interactions not dealing with host manipulation. To explore the implications of this oversight, we synthesized available literature to identify patterns in virus effects among pathogens with shared transmission mechanisms and discussed the results of this synthesis in the context of molecular and environmental constraints on virus evolution, limitations of existing studies, and prospects for future research.

A growing number of studies suggest that plant viruses manipulate host plant phenotypes to increase transmission-conducive behaviors by vectors. Studies on this phenomenon frequently omit examination of interactions that occur after vectors acquire virions, which provides an incomplete understanding of the ecology of plant virus manipulation. Here, by taking a full factorial approach that considered both the infection status of the host (Montia perfoliata) and viruliferous status of the aphid (Myzus persicae), we explored the effects of a circulative, non-propagative virus (Turnip yellows virus [TuYV]) on a suite of behavior and performance metrics that are relevant for virus transmission. Our results demonstrate that viruliferous aphids exhibited an increased velocity of movement and increased activity levels in locomotor and dispersal-retention assays. They also had increased fecundity and showed a capacity to more efficiently exploit resources by taking less time to reach the phloem and ingesting more sap, regardless of plant infection status. In contrast, non-viruliferous aphids only exhibited enhanced fecundity and biomass on TuYV-infected hosts, and had overall reduced dispersal and locomotor activity relative to viruliferous aphids. In this pathosystem, post-acquisition effects were stronger and more conducive to virus transmission than the purely pre-acquisition effects mediated by virus effects on the host plant. Our study provides additional support for the hypothesis that virus manipulation of vector behavior includes both pre- and post-acquisition effects and demonstrates the importance of considering both components when studying putative virus manipulation strategies.

Cowpea (Vigna unguiculata) is one of the most important crops in semiarid areas of the world, where it thrives in hot, dry conditions. While cowpea is able to withstand abiotic stresses, it suffers serious losses from biotic antagonists, including infestation by the cowpea aphid (Aphis craccivora). Cowpea aphid infestations are highly destructive, especially on young plants. However, it is unclear whether cowpea aphid damage is the result of aphids having phytotoxic effects on their hosts, or simple density effects. To better understand cowpea aphid damage and the potential for resistance traits to mitigate aphid impacts, we evaluated phenotypic changes in cowpea in response to variable aphid densities and systemic versus local infestations. Low aphid densities induced leaf distortions and pseudogalling, suggesting that cowpea aphids are phytotoxic to cowpea. Resistance to the cowpea aphid has been previously identified in an African cowpea germplasm, and near isogenic lines (NILs) containing resistance quantitative trait loci (QTL) were generated in the California blackeye cultivar background. Using a series of performance assays, we determined that resistance conferred by the two QTL counteracts aphid phytotoxicity and severely limits aphid growth and fecundity. Using choice assays, a preference by cowpea aphids for the susceptible NIL was observed. Electrical penetration graph analysis revealed that the resistance phenotype includes weak surface level deterrence and strong phloem-based resistance that manifests during the sap ingestion phase. Our study provides evidence of phytotoxic traits in A. craccivora while identifying a viable means of counteracting aphid damage and reproductive potential through resistance.