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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Emerging Pests and Pathogens Research » Research » Publications at this Location » Publication #321707

Title: Host plants indirectly influence plant virus transmission by altering gut cysteine protease activity of aphid vectors

Author
item PINHEIRO, PATRICIA - Cornell University - New York
item GHANIM, MURAD - Volcani Center (ARO)
item ALEXANDER, MARIKO - Cornell University - New York
item REBELO, ANA RITA - Boyce Thompson Institute
item SANTOS, ROGERIO - Boyce Thompson Institute
item ORSBURN, BENJAMIN - Thermo Fisher Scientific
item Gray, Stewart
item Heck, Michelle

Submitted to: Molecular and Cellular Proteomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2016
Publication Date: 12/8/2016
Citation: Pinheiro, P., Ghanim, M., Rebelo, A., Santos, R., Orsburn, B.C., Gray, S.M., Cilia, M. 2016. Host plants indirectly influence plant virus transmission by altering gut cysteine protease activity of aphid vectors. Molecular and Cellular Proteomics. DOI: 10.1074/mcp.M116.063495.

Interpretive Summary: Potato leaf roll virus (PLRV) is transmitted between plants by aphids, sap-sucking insects. The green peach aphid, the major insect vector of PLRV, colonizes a variety of plant species, many of which are not hosts of the virus. PLRV and related plant viruses must circulate throughout the aphid body prior to transmission to a new host plant. Despite the extensive knowledge of environmental, microbial, and insect genetic factors regulating plant virus transmission by aphids, little is known about how aphid-plant interactions influence virus transmission. In this study, we characterized the effect of different host plants on the ability of the green peach aphid to transmit PLRV. Unexpectedly, we found that aphids reared on turnip, a non-host of PLRV, transmitted the virus much less efficiently as compared to aphids reared on physalis, a weedy host of PLRV. Our experiments revealed that digestive enzymes that break down proteins at specific residues play an indirect role in regulating virus transmission by aphids. This is the first study to show that the virus transmission efficiency of an aphid can be host-dependent, and to demonstrate that by modulating the activity of aphid gut enzymes, the ability of an aphid to transmit PLRV can be reduced. The discovery may pave the way towards the development of novel strategies to control the spread of aphid-transmitted viruses within a crop.

Technical Abstract: 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 to the weed physalis, a transient effect caused by a host-switch response. A trend of higher PLRV titer in physalis-reared aphids as compared to turnip-reared aphids was observed at 24h and 72h after virus acquisition. The major difference in the proteomes of these aphids was the upregulation 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 is near complete co-localization 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 decreases 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.