Exportin 1 is required for the reproduction and maize mosaic virus accumulation in its insect vector Peregrinus maidis

Abstract

Exportin 1 (XPO1) is the major karyopherin-{beta} nuclear receptor mediating the nuclear export of hundreds of proteins and some classes of RNA and regulates several critical processes in the cell, including but not limited to, cell-cycle progression, transcription, translation, oncogenesis and longevity. Viruses have co-opted XPO1 to promote nucleocytoplasmic transport of viral proteins and RNA. Maize mosaic virus (MMV) is an Alphanucleorhabdovirus 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 simultaneously and 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 to the guts of adult females. Survival rate was significantly lower for PmXPO1 knockdown females, compared to controls, but no effect was observed for males. Adult females with PmXPO1 knockdown were heavier and had a larger abdomen compared to controls at 4, 8 and 12 days after dsRNA microinjection. Consistent with an increase in weight, glyceride content specifically and significantly increased in PmXPO1 knockdown female planthoppers. Ovary development was significantly inhibited, and mature eggs were not observed in adult females with PmXPO1 knockdown. Consistent with a major role of PmXPO1 in ovary function and egg production, oviposition and egg hatch in plants was dramatically reduced in dsRNA PmXPO1 treated insects compared with control. Altogether, 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.