A polerovirus, Potato leafroll virus, alters plant–vector interactions using three viral proteins

Potato leafroll virus (PLRV), genus Polerovirus, family Luteoviridae, is a major pathogen of potato worldwide. PLRV is transmitted among host plants by aphids in a circulative–nonpropagative manner. Previous studies have demonstrated that PLRV infection increases aphid fecundity on, and attraction to, infected plants as compared to controls. However, the molecular mechanisms mediating this relationship are still poorly understood. In this study, we measured the impact of PLRV infection on plant–aphid interactions and plant chemistry in two hosts: Solanum tuberosum and Nicotiana benthamiana. Our study demonstrates that PLRV infection attenuates the induction of aphid‐induced jasmonic acid and ethylene in S. tuberosum and N. benthamiana. Using transient expression experiments, insect bioassays and chemical analysis, we show that expression of three PLRV proteins (P0, P1, and P7) mediate changes in plant–aphid interactions and inhibition of aphid‐induced jasmonic acid and ethylene in N. benthamiana. This study enhances our understanding of the plant‐vector‐pathogen interface by elucidating new mechanisms by which plant viruses transmitted in a circulative manner can manipulate plant hosts. Our study demonstrates that Potato leafroll virus inhibits the induction of aphid‐induced phytohormones using at least three viral proteins (P0, P1, and P7). This is the first time that individual viral proteins of a circulative–nonpropagative virus have been shown to alter host physiology and, in turn, aphid behaviour and fecundity.