Infection with a plant virus modifies vector feeding behavior

Abstract

Vector infection by some animal-infecting parasites results in altered feeding that enhances transmission. Modification of vector behavior is of broad adaptive significance, as parasite fitness relies on passage to a new host, and vector feeding is nearly always essential for transmission. Although several plant viruses infect their insect vectors, we have shown that vector infection by a plant virus alters feeding behavior. Here we show that infection with Tomato spotted wilt virus (TSWV), type member of the only plant-infecting genus in the Bunyaviridae, alters the feeding behavior of its thrips vector, Frankliniella occidentalis (Pergande). Male thrips infected with TSWV fed more than uninfected males, with the frequency of all feeding behaviors increasing by up to threefold, thus increasing the probability of virus inoculation. Importantly, infected males made almost three times more noningestion probes (probes in which they salivate, but leave cells largely undamaged) compared with uninfected males. A functional cell is requisite for TSWV infection and cell-to-cell movement; thus, this behavior is most likely to establish virus infection. Some animalinfecting members of the Bunyaviridae (La Crosse virus and Rift Valley fever virus) also cause increased biting rates in infected vectors. Concomitantly, these data support the hypothesis that capacity to modify vector feeding behavior is a conserved trait among plant-and animal-infecting members of the Bunyaviridae that evolved as a mechanism to enhance virus transmission. Our results underscore the evolutionary importance of vector behavioral modification to diverse parasites with host ranges spanning both plant and animal kingdoms. virus evolution | Tospovirus | virus-vector interactions

Incidence of viruses and virus-like diseases of watermelons and pumpkins in Uganda, a hitherto none-investigated pathosystem

“…A classic example is demonstrated under a natural ecosystem by introducing annual grass species that have overturned the dominance of perennial native bunchgrasses in California grasslands via increased infection with aphid-borne Barley/Cereal yellow dwarf viruses (Malmstrom et al, 2005;Borer et al, 2007;HilleRisLambers et al, 2010). Also, feeding preferences or feeding behaviour of insect vectors of plant viruses can be altered after exposure to infected plants and acquisition of virus (Stafford et al, 2011;Ingwell et al, 2012;MorenoDelafuente et al, 2013;Rajabaskar et al, 2014). In these contexts, a much higher abundance of aphids was observed on watermelons than on pumpkins in Uganda (Our unpublished data), and whether or not it has implications with increased virus impact on pumpkins is an interesting subject of our future studies.…”

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…Indeed, differing persistence times might be a major explanation for the observation that manipulation effects are more frequently reported for intermediate than for final hosts, at least as long as all hosts are animals (Holmes and Bethel, 1972). Plant pathogens, by contrast, require mobile vectors for their dispersal among their immobile final hosts and, therefore, frequently manipulate the quality of their host plant for the vectors (Belliure et al, 2010;Mauck et al, 2010Mauck et al, , 2014aLuan et al, 2013;Shi et al, 2013) as well as the feeding decisions that are taken by their vectors (Stafford et al, 2011;Ingwell et al, 2012;Mann et al, 2012;Fang et al, 2013;Rajabaskar et al, 2014). These changes can be very fine-tuned: for example, plant viruses with a persistent mode of transmission require vectors to feed for a prolonged period of time on infected hosts and, thus, usually tend to improve the quality of the host plants for the vectors.…”

“…Because plants are sessile, many pathogens of plants use the same strategies for their transmission as the agents of vectorborne human diseases (Guiguet et al, 2016) and, for example, change the behavior of their vectors to enhance transmission from infected to healthy plants hosts (Stafford et al, 2011;Ingwell et al, 2012;Rajabaskar et al, 2014), alter the emission of volatile organic compounds (VOCs) from the infected host (Mauck et al, 2010), or enhance the nutritional quality of the infected plant for herbivores that serve as their vectors (Fang et al, 2013;Luan et al, 2013;Shi et al, 2014). One of the most intriguing examples is Cucumber mosaic virus: the bouquet of VOCs emitted by infected plants is altered, making the plants more attractive to the aphids that vector this virus, even though the nutritional quality of infected plants is lower (Mauck et al, 2010).…”

“…For example, Tomato spotted wilt virus augments the frequency of all feeding behaviors in infected males of its thrips vector (Stafford et al, 2011), and Candidatus Liberibacter asiaticus makes the odor of infected citrus plants initially more attractive for its psyllid vector but then, after virus acquisition, causes psyllids to disperse to non-infected plants (Mann et al, 2012). Similarly, Tomato yellow leaf curl virus enhances the attractiveness of infected tomato plants to virus-free whiteflies (B. tabaci), whereas infected whiteflies lose the capacity to distinguish between infected and healthy host plants (Fang et al, 2013).…”

Plant Virus Ecology: A Glimpse of Recent Accomplishments

“…Further research revealed that the interaction between virus and vector was mutually beneficial for each other specifically for the biotype Q only (Pan et al, 2013). Similarly in thrips interaction, the feeding behavior of male Frankliniella occidentalis (Pergande, 1985) infected by TSWV (Tomato spotted wilt virus) was changed thus influencing the transmission of the virus (Stafford et al, 2011). Natural enemies of insect vectors also play an important role in altering virus spread patterns by using different strategic methods.…”