Evolutionary Determinants of Host and Vector Manipulation by Plant Viruses

Abstract

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.

Virus mediated trophic interactions between aphids and their natural enemies

“…In the pea aphid, Acyrthosiphon pisum, infection with the bacterial endosymbiont Hamiltonella defensa induces reduction in aphid defensive behaviours (Dion et al 2011, Polin et al 2014) and by consequence, increases in predation rates (Polin et al 2014). Altered behaviours were also observed in aphids infected with entomopathogenic fungi (Jensen et al 2001) and plant viruses acquired from infected host plants (Mauck et al 2018). As viral infection can be associated with physiological costs for aphids, this may induce some reductions in aphid defensive behaviours (Dion et al 2011).…”

Evidence of adaptive host and vector manipulation by plant viruses revealed through combined meta-analysis and modeling approaches

“…This evidence is essential for understanding 117 manipulation because many of these parasites and their hosts are intractable for functional 118 genomics work to identify genes, and gene targets that may underlie adaptive manipulation 119 (Heil 2016). Convergence of virus effects in the absence of phylogenetic relatedness 120 provides indirect evidence in support of particular effects being the product of virus 121 adaptations rather than by-products of pathology (Thomas et al 2005;Mauck et al 2018). 122 123 Here, we used virus traits associated with transmission as a framework for quantifying the 124 adaptive significance of virus effects on host phenotypes using meta-analysis.…”

“…In reality, nearly 70% of the NPL viruses 666 included in the meta-analysis are transmissible by more than 20 vector species, and all are 667 transmissible by 5 or more vector species (Fig. S1, electronic Mauck et al 2018). But we can 676 speculate that the difference in transmission opportunities between PL and NPL viruses will 677 significantly influence the relative fitness benefits of host manipulation for these virus trait 678 groups.…”

“…Incorporating new pathosystems and 706 ecological dimensions into future empirical and theoretical work is therefore necessary to 707 understand the frequency and relevance of virus manipulation in real-world scenarios. The 708 number of researchers studying this topic is growing (Mauck et al 2018, as is interest 709 in finding ways to manage manipulative effects of viruses in agricultural contexts (Bak et al 710 25 2019) and understanding their importance in wild systems (Alexander et al 2014). Tackling 711 these ambitious research directions requires integrative approaches informed by virology, 712 ecology, entomology, and plant biology.…”

An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

“…persicae to colonize specific plant species (22). Interestingly, CathB genes are also differentially regulated in aphids on healthy versus those on virus-infected plants (23) and viruses are known to modulate plant defense responses (24,25). These studies provide evidence that M. persicae has the ability to perceive the host plant status and adjust its gene expression accordingly.…”