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

Carr, John P., Tungadi, Trisna, Donnelly, Ruairí, Bravo-Cazar, Ana, Rhee, Sun-Ju, Watt, Lewis G., Mutuku, J. Musembi, Wamonje, Francis O., Murphy, Alex M., Arinaitwe, Warren, Pate, Adrienne E., Cunniffe, Nik J., Gilligan, Christopher A.
Virus research 2020 v.277 pp. 197845
Aphidoidea, Cucumber mosaic virus, Potyviridae, feeding behavior, hosts, induced resistance, insect infestations, insects, mathematical models, nutrients, plant biochemistry, plant viruses, stylets, tissues, viral proteins, virion, viruses, volatile organic compounds
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.