RNAi‐mediated knockdown of exportin 1 negatively affected ovary development, survival and maize mosaic virus accumulation in its insect vector Peregrinus maidis

Exportin 1 (XPO1) is the major karyopherin‐β nuclear receptor mediating the nuclear export of hundreds of proteins and some classes of RNA and regulates several critical processes in the cell, including cell‐cycle progression, transcription and translation. Viruses have co‐opted XPO1 to promote nucleocytoplasmic transport of viral proteins and RNA. Maize mosaic virus (MMV) is a plant‐infecting rhabdovirus transmitted in a circulative propagative manner by the corn planthopper, Peregrinus maidis. MMV replicates in the nucleus of plant and insect hosts, and it remains unknown whether MMV co‐opts P. maidis XPO1 (PmXPO1) to complete its life cycle. Because XPO1 plays multiple regulatory roles in cell functions and virus infection, we hypothesized that RNAi‐mediated silencing of XPO1 would negatively affect MMV accumulation and insect physiology. Although PmXPO1 expression was not modulated during MMV infection, PmXPO1 knockdown negatively affected MMV accumulation in P. maidis at 12 and 15 days after microinjection. Likewise, PmXPO1 knockdown negatively affected P. maidis survival and reproduction. PmXPO1 exhibited tissue‐specific expression patterns with higher expression in the ovaries compared with the guts of adult females. Survival rate was significantly lower for PmXPO1 knockdown females, compared with controls, but no effect was observed for males. PmXPO1 knockdown experiments revealed a role for PmXPO1 in ovary function and egg production. Oviposition and egg hatch on plants were dramatically reduced in females treated with dsRNA PmXPO1. These results suggest that PmXPO1 is a positive regulator of P. maidis reproduction and that it plays a proviral role in the insect vector supporting MMV infection. XPO1 plays multiple regulatory roles in cell functions, and RNAi‐mediated silencing of XPO1 negatively affected P. maidis physiology in a sex‐specific manner, including increased weight, lower survival and reproduction. dsXPO1‐treated females exhibited poorly developed ovarioles with no mature eggs or oocytes being observed, leading to a significant reduction in oviposition and egg hatch on plants. PmXPO1 knockdown negatively affected MMV accumulation in P. maidis males and females at 12 and 15 days after microinjection. These results suggest that XPO1 plays a proviral role during a plant rhabdovirus infection in its insect vector.