Virus and helper component interactions favor the transmission of recombinant potato virus Y strains

Authors: MONDAL, SHAONPIUS - Oak Ridge Institute For Science And Education (ORISE); Wintermantel, William - Bill; Gray, Stewart

Submitted to: Journal of General Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2021
Publication Date: 6/23/2021
Citation: Mondal, S., Wintermantel, W.M., Gray, S.M. 2021. Virus and helper component interactions favour the transmission of recombinant potato virus Y strains. Journal of General Virology. 102(6). https://doi.org/10.1099/jgv.0.001620.
DOI: https://doi.org/10.1099/jgv.0.001620

Interpretive Summary: In recent years, three recombinant strains of potato virus Y have displaced the ordinary strain on the virus, and emerged as the predominant PVY strains infecting the U.S. potato crop. Our previous work showed that recombinant strains were transmitted more efficiently than the ordinary strain when they were acquired sequentially, regardless of acquisition order. This suggested that the recombinant strains may bind more effectively within the aphids that transmit these viruses. We also demonstrated that one particular recombinant strain binds more effectively to the aphid stylet than the ordinary strain when aphids fed on a mixture of the two strains. We separated virus particles and viral proteins required for aphid transmission (called helper component or HC), mixed them in different combinations, and then fed them to aphids in order to understand why transmission favors recombinant strains. Variation in aphid transmission efficiency was observed among treatments. The HC of one particular recombinant strain facilitated the transmission of that strain only, while the HCs of the ordinary strain and one other recombinant strain facilitated the transmission of all strains tested. Thus, strain–HC interactions may have contributed to the increase in the recombinant strains affecting the U.S. potato crop. This is the first report of helper component–strain specificity within a potyvirus species.

Technical Abstract: Several recombinant strains of potato virus Y, notably PVYNWi, PVYNTN and PVYN:O have displaced the ordinary strain, PVYO in recent years and emerged as the predominant PVY affecting the U.S. potato crop. Our previous work showed that recombinant strains were transmitted more efficiently than PVYO when they were acquired sequentially, regardless of acquisition order, and that PVYNTN binds preferentially to the aphid stylet over PVYO when aphids feed on mixture of PVYO and PVYNTN. In this research, we separated virus and active helper component proteins (HC), mixed them in homologous and heterologous combinations, and then fed them to aphids using Parafilm® sachets in order to understand the mechanism of this transmission bias and preferential virus binding. Mixtures of PVYO HC with either recombinant virus, PVYN:O or PVYNTN, resulted in efficient transmission. PVYN:O HC also facilitated the transmission of PVYO and PVYNTN, albeit with reduced efficiency. PVYNTN HC failed to facilitate transmission of either PVYO or PVYN:O. When PVYO HC or PVYN:O HC was mixed with equal amounts of the two viruses, both viruses in all combinations were transmitted at high efficiencies. In contrast, no transmission occurred when combinations of viruses were mixed with PVYNTN HC. Further study evaluated transmission using serial dilutions of purified virus mixed with similar amounts of HCs. While PVYNTN HC only facilitated the transmission of the homologous virus, the HCs of PVYO and PVYN:O facilitated the transmission of all strains tested. Thus, strain–HC interactions may have contributed to the increase in the recombinant strains affecting the U.S. potato crop. This is the first report of helper component–strain specificity within a potyvirus species.