SatRNA-mediated exacerbation of disease symptoms in plants reduces virus transmission potential by aphids

Plant viruses have evolved adaptations that enable them to alter host cues, thereby facilitating their replication and efficient transmission by insect vectors. Satellite RNAs (satRNAs), which accompany certain plant RNA viruses and are dependent on them for replication and transmission, can change the progression of pathogenesis and the expression of disease symptoms. This study aimed to analyse how the change in the course of infection by satRNA (exacerbation or mitigation of pathogenesis) impacts the subsequent stages of virus transmission. We hypothesised that satRNAs influence insect behaviour toward infected plants depending on their effect on pathogenesis progress; specifically, a significant disease exacerbation reduces plant attractiveness to aphids, whereas symptom mitigation promotes attraction.

Using peanut stunt virus (PSV) and cucumber mosaic virus (CMV), and their satRNAs, which induce divergent infection symptoms on Nicotiana benthamiana or Solanum lycopersicum plants, olfactometry, electrical penetration graph (EPG) monitoring, virus acquisition and transmission by Myzus persicae were analysed. The results showed that satRNA, naturally associated with the helper virus, that alleviate disease symptoms caused the plants to be more attractive to the insect vectors. On the other hand, the presence of satRNAs leading to symptom exacerbation reduced plant attractiveness and discouraged phloem feeding. However, acquisition effects were host-dependent: while symptom-exacerbating satRNAs generally reduced acquisition, nc-satRNA markedly enhanced CMV acquisition from N. benthamiana. Moreover, virus transmission was significantly reduced only in S. lycopersicum.

These findings suggest that symptom-attenuating satRNAs have greater capacity to persist in the environment by limiting disease damage in host plants and maintaining plant attractiveness to aphid vectors, thereby facilitating virus acquisition and transmission. In contrast, symptom-exacerbating satRNA variants appear not only to diminish the number of cells available for viral replication due to severe symptoms but also to reduce plant palatability and to impair vector feeding and thus virus transmission, particularly in crop hosts such as S. lycopersicum, which may limit their environmental persistence. Together, these results underscore the epidemiological relevance of satRNA-mediated symptom modulation as a factor shaping virus spread in natural and agricultural settings.