Abstract

The green peach aphid, Myzus persicae, is a vector of the Potato leafroll virus (PLRV, Luteoviridae), transmitted exclusively by aphids in a circulative manner. PLRV transmission efficiency was significantly reduced when a clonal lineage of M. persicae was reared on turnip as compared with the weed physalis, and this was a transient effect caused by a host-switch response. A trend of higher PLRV titer in physalis-reared aphids as compared with turnip-reared aphids was observed at 24 h and 72 h after virus acquisition. The major difference in the proteomes of these aphids was the up-regulation of predicted lysosomal enzymes, in particular the cysteine protease cathepsin B (cathB), in aphids reared on turnip. The aphid midgut is the site of PLRV acquisition, and cathB and PLRV localization were starkly different in midguts of the aphids reared on the two host plants. In viruliferous aphids that were reared on turnip, there was near complete colocalization of cathB and PLRV at the cell membranes, which was not observed in physalis-reared aphids. Chemical inhibition of cathB restored the ability of aphids reared on turnip to transmit PLRV in a dose-dependent manner, showing that the increased activity of cathB and other cysteine proteases at the cell membrane indirectly decreased virus transmission by aphids. Understanding how the host plant influences virus transmission by aphids is critical for growers to manage the spread of virus among field crops.

Highlights

  • From the ‡Department of Entomology, Cornell University, Ithaca, New York 14853; §Boyce Thompson Institute for Plant Research, Ithaca, New York 14853; ¶Embrapa Rice and Beans, Santo Antonio de Goias 171, Brazil; ʈDepartment of Entomology, Volcani Center, Bet Dagan 5025001, Israel; **Plant Pathology and Plant Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, New York; ‡‡Thermo Fisher, San Jose, California; §§USDA Agricultural Research Service, Emerging Pests and Pathogens Research Unit, Robert W

  • Biochemical, molecular, proteomic, and imaging approaches, we show that high levels of cysteine proteases at the cell membrane in aphids reared on turnip are indirectly responsible for the host-dependent change in the virus transmission phenotype in M. persicae

  • A significant growth reduction was reported by Rahbeand collaborators [57] when they fed M. persicae on transgenic oilseed rape plants (Brassica napus) expressing the cysteine protease inhibitor oryzacystatin, which suggests that cathepsin activity in the aphid is required for proper growth and low levels of cathepsin impairs aphid growth

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Summary

Introduction

Biochemical, molecular, proteomic, and imaging approaches, we show that high levels of cysteine proteases at the cell membrane in aphids reared on turnip are indirectly responsible for the host-dependent change in the virus transmission phenotype in M. persicae. We tested whether the difference in PLRV transmission could be because of a difference in the aphids’ ability to acquire the virus when they are reared on different host plants by comparing PLRV genomic RNA levels in T- and P-Myzus after gut clearing on artificial diets.

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