Specific and Spillover Effects on Vectors Following Infection of Two RNA Viruses in Pepper Plants

Abstract

Mixed infection of plant viruses is ubiquitous in nature and can affect virus–plant–vector interactions differently than single virus infection. While several studies have examined virus–virus interactions involving mixed virus infection, relatively few have examined effects of mixed virus infection on vector preference and fitness, especially when multiple vectors are involved. This study explored how single and mixed viral infection of a non-persistently transmitted cucumber mosaic virus (CMV) and propagative and persistently-transmitted tomato spotted wilt orthotospovirus (TSWV) in pepper, Capsicum annum L., influenced the preference and fitness of their vectors, the green peach aphid, Myzus persicae (Sulzer), and the tobacco thrips, Frankliniella fusca (Hinds), respectively. In general, mixed infected plants exhibited severe symptoms compared with individually infected plants. An antagonistic interaction between the two viruses was observed when CMV titer was reduced following mixed infection with TSWV in comparison with the single infection. TSWV titer did not differ between single and mixed infection. Myzus persicae settling preference and median developmental were not significantly different between CMV and/or TSWV-infected and non-infected plants. Moreover, M. persicae fecundity did not differ between CMV-infected and non-infected pepper plants. However, M. persicae fecundity was substantially greater on TSWV-infected plants than non-infected plants. Myzus persicae fecundity on mixed-infected plants was significantly lower than on singly-infected and non-infected plants. Frankliniella fusca fecundity was higher on CMV and/or TSWV-infected pepper plants than non-infected pepper plants. Furthermore, F. fusca-induced feeding damage was higher on TSWV-infected than on CMV-infected, mixed-infected, or non-infected pepper plants. Overall, our results indicate that the effects of mixed virus infection on vectors were not different from those observed following single virus infection. Virus-induced host phenotype-modulated effects were realized on both specific and non-specific vectors, suggesting crosstalk involving all vectors and viruses in this pathosystem. The driving forces of these interactions need to be further examined. The effects of interactions between two viruses and two vectors towards epidemics of one or both viruses also need to be examined.

A Review on Transcriptional Responses of Interactions between Insect Vectors and Plant Viruses

“…Currently, there are four described major modes of virus transmission, ranging from non-persistent to persistent-propagative [ 36 , 37 ]. Irrespective of the mode of transmission, many plant viruses infecting their host plants tend to attract their associated vectors [ 97 , 100 , 101 ]. However, the arrestment duration of their vectors ranging from a brief period (without providing long-term fitness benefits) to a prolonged period (with provision of long-term fitness benefits) is dependent on the mode of transmission [ 97 ].…”

Interactions between insect vectors and plant pathogens span the parasitism–mutualism continuum

“… Frankliniella fusca tomato spotted wilt virus (TSWV)fecunditylikely both[37] Capsicum annuum L . Myzus persicae (green peach aphid)cucumber mosaic virus (CMV)fecundityindirect[37] Capsicum annuum L . Myzus persicae tomato spotted wilt virus (TSWV)fecunditylikely both[37] Cucurbita pepo (pumpkin) Aphis gossypii (melon aphid)papaya ring spot virus (PRSV)fecundityindirect[38] Cucurbita pepo Bemisia tabaci (whitefly)squash vein yellowing virus (SqVYV)adult longevity, fecundityindirect[11] Glycine max (soya bean) Aphis glycines (soya bean aphid)soya bean mosaic virus (SMV)fecundityindirect[39,40] Gossypium hirsutum (cotton) Bemisia tabaci (whitefly)tomato yellow leaf curl China virus (TYLCCNV)fecunditydirect[41] Gossypium hirsutum Bemisia tabaci tomato yellow leaf curl virus (TYLCV)adult longevity, fecunditylikely both[42] Hordeum vulgare (barley) Laodelphax striatellus (small brown planthopper)maize Iranian mosaic virus (MIMV)adult longevity, fecunditydirect[43] Medicago sativa (alfalfa) Acyrthosiphon pisum (pea aphid)bean leafroll virus (BLRV)survivallikely both…”

Viruliferous and non‐viruliferous aphids behave differently to enhance the spread of the virus

“…These changes may affect the host plant, which indirectly affects the vector performance. For example, some plant viruses induce changes in the host plants that ultimately affect the insect vector settling and feeding behaviour (Mauck et al., 2010; Gautam et al., 2020b). Around 70 years ago, Kennedy reported the first impact of acute plant viruses on insect behaviour (Kennedy, 1951).…”