Modelling and manipulation of aphid-mediated spread of non-persistently transmitted viruses

Abstract

Aphids vector many plant viruses in a non-persistent manner i.e., virus particles bind loosely to the insect mouthparts (stylet). This means that acquisition of virus particles from infected plants, and inoculation of uninfected plants by viruliferous aphids, are rapid processes that require only brief probes of the plant's epidermal cells. Virus infection alters plant biochemistry, which causes changes in emission of volatile organic compounds and altered accumulation of nutrients and defence compounds in host tissues. These virus-induced biochemical changes can influence the migration, settling and feeding behaviours of aphids. Working mainly with cucumber mosaic virus and several potyviruses, a number of research groups have noted that in some plants, virus infection engenders resistance to aphid settling (sometimes accompanied by emission of deceptively attractive volatiles, that can lead to exploratory penetration by aphids without settling). However, in certain other hosts, virus infection renders plants more susceptible to aphid colonisation. It has been suggested that induction of resistance to aphid settling encourages transmission of non-persistently transmitted viruses, while induction of susceptibility to settling retards transmission. However, recent mathematical modelling indicates that both virus-induced effects contribute to epidemic development at different scales. We have also investigated at the molecular level the processes leading to induction, by cucumber mosaic virus, of feeding deterrence versus susceptibility to aphid infestation. Both processes involve complex interactions between specific viral proteins and host factors, resulting in manipulation or suppression of the plant's immune networks.

Keywords: Argonaute; Epidemiology; Inoculation; Insect vector; Markov chain; Virus acquisition.

Fig. 1

A cartoon depiction of the ‘attract and deter’ virally-induced plant phenotype. Certain non-persistently-transmitted plant viruses induce metabolic changes in infected plants that results in the emission of aphid-attracting volatile organic chemical (VOC) blends. In this scenario, an aphid may be attracted to an infected plant but brief feeding and sampling of epidermal cell contents reveals to the insect that virus infection has induced the accumulation of distasteful compounds. This deters the aphid from settling and will cause it to move on to find a more suitable host. During the sampling feed, viral inoculum will have been acquired (depicted by the icosahedron). Thus, induction of the ‘attract and deter’ virally-induced phenotype will increase the likelihood of an aphid transmitting inoculum to a non-infected plant. Based on findings and analyses by Carmo-Sousa et al. (2014), Donnelly et al. (2019); Mauck et al. (2010), and Westwood et al. (2013).

Fig. 2

A cartoon depiction of the predicted effects of ‘attract and deter’ versus ‘retain’ virally-induced plant phenotypes on transmission of non-persistently aphid-vectored viruses. (A) The outputs of epidemiological modelling by Donnelly et al. (2019) support the idea that a virally-induced ‘attract and deter’ plant phenotype will engender relatively rapid local spread of virus (upper panel), whereas induction of a ‘retain’ phenotype (lower panel), will not. However, they also predict virus transmission promoted by the ‘attract and deter’ phenotype will be self-limiting since aphids will reproduce less if not settled and be exposed to increased risks of predation as they travel between plants, leading to decreased vector density. (B) It is predicted that a virally-induced ‘retain’ plant phenotype resulting from increased nutritional quality or decreased resistance to aphid colonisation will encourage aphids to settle, reproduce and become crowded (Donnelly et al., 2019). Crowding induces increased production of winged (alate) aphids (Braendle et al., 2006). (C) The modelling of Donnelly et al. (2019) predicts that enhanced production of alates on plants expressing a virally-induced ‘retain’ phenotype will result in longer-distance transmission. Although this enhancement in virus transmission may take longer to occur than that driven by the ‘attract and deter’ virally-induced plant phenotype, it was suggested that it may be more effective in launching epidemics (Donnelly et al., 2019).