Symptom-modulating satRNAs of cucumoviruses affect the orientation and feeding behaviour of Myzus persicae

Abstract

Plant viruses evolved mechanisms to manipulate host plants to replicate and be efficiently transmitted by insect vectors. In the context of non-persistently transmitted viruses, an important strategy is to change the plants metabolism to attract the vectors, and subsequently repel viruliferous insects from the infected plants to facilitate the virus transmission to neighbouring plants. The presence of satellite RNAs (satRNAs), which accompany certain plant RNA virus species and strains, leads to changes in the host plants, such as alterations in the virus-induced infection symptoms, either exacerbating or attenuating them. This study aimed to analyse the influence of satRNAs on the orientation and feeding behaviour of the cucumovirus insect vector - Myzus persicae, which might consequently contribute to the virus transmission efficiency. The hypothesis behind this study was that satRNAs of cucumoviruses alter these insect activities toward virus-infected plants, and strongly symptom-deteriorating satRNAs might negatively affect the attractiveness of the infected plants for aphids. Using two cucumoviruses, peanut stunt virus (PSV) and cucumber mosaic virus (CMV), and their satRNAs, which induce divergent infection symptoms, olfactometry and electrical penetration graph (EPG) monitoring analyses were performed. The results showed that satRNAs which presence leads to disease symptom exacerbation might alter the orientation behaviour of aphids by reducing the attractiveness of the plants and discouraging aphids from feeding. This phenomenon may contribute to the better persistence in the environment of satRNAs alleviating disease symptoms compared to the worsening ones, benefiting the virus by not destroying the plant and prolonging the virus exposure to insect vectors.