A plant virus manipulates the long-winged morph of insect vectors.

Abstract

Wing dimorphism of insect vectors is a determining factor for viral long-distance dispersal and large-area epidemics. Although plant viruses affect the wing plasticity of insect vectors, the potential underlying molecular mechanisms have seldom been investigated. Here, we found that a planthopper-vectored rice virus, rice stripe virus (RSV), specifically induces a long-winged morph in male insects. The analysis of field populations demonstrated that the long-winged ratios of male insects are closely associated with RSV infection regardless of viral titers. A planthopper-specific and testis-highly expressed gene, <i>Encounter</i>, was fortuitously found to play a key role in the RSV-induced long-winged morph. Encounter resembles malate dehydrogenase in the sequence, but it does not have corresponding enzymatic activity. <i>Encounter</i> is upregulated to affect male wing dimorphism at early larval stages. <i>Encounter</i> is closely connected with the insulin/insulin-like growth factor signaling pathway as a downstream factor of <i>Akt</i>, of which the transcriptional level is activated in response to RSV infection, resulting in the elevated expression of <i>Encounter</i>. In addition, an RSV-derived small interfering RNA directly targets <i>Encounter</i> to enhance its expression. Our study reveals an unreported mechanism underlying the direct regulation by a plant virus of wing dimorphism in its insect vectors, providing the potential way for interrupting viral dispersal.