Polerovirus N-terminal readthrough domain structures reveal novel molecular strategies for mitigating virus transmission by aphids

Authors: SCHILTZ, CARL - Cornell University; Wilson, Jennifer - Jenny; HOSFORD, CHRISTOPHER - Cornell University; ADAMS, MYFANWY - Cornell University; PREISING, STEPHANIE - Cornell University; Deblasio, Stacy; MACCLEOD, HANNAH - Former ARS Employee; VEN ECK, JOYCE - Boyce Thompson Institute; Heck, Michelle; CHAPPIE, JOSHUA - Cornell University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2022
Publication Date: 10/26/2022
Citation: Schiltz, C.J., Wilson, J.R., Hosford, C., Adams, M.C., Preising, S.E., Deblasio, S.L., Maccleod, H.J., Ven Eck, J., Heck, M.L., Chappie, J.S. 2022. Polerovirus N-terminal readthrough domain structures reveal novel molecular strategies for mitigating virus transmission by aphids. Nature Communications. 13:6368. https://doi.org/10.1038/s41467-022-33979-2.
DOI: https://doi.org/10.1038/s41467-022-33979-2

Interpretive Summary: Many viruses that infect plants rely on an insect vector for plant-to-plant spread. In this work, we focused on a group of insect-transmitted viruses, the poleroviruses, which cause economically important diseases of vegetables and other crops, including cotton. We determined the structure of a protein on the surface of these viruses that is crucial for the virus to be picked up and transmitted by its insect vector. We also found that this protein could be used to block virus transmission: when the insects feed on this protein they can no longer effectively transmit the virus. This protein was found to be a powerful inhibitor of virus transmission across three different delivery strategies. Moreover, the research revealed that variants of this protein are lethal to the insects. The results show a new way to block the transmission of these economically important viruses as well as a new way to kill the insect vectors. The work impacts not only scientists who want to understand these viruses but also industry and, ultimately, growers who are looking for new ways to help manage these destructive viral pathogens.

Technical Abstract: Poleroviruses, enamoviruses, and lutoeviruses are icosahedral, positive sense RNA viruses that cause economically important diseases in food and fiber crops. They are transmitted by phloem-feeding aphids in a circulative manner that involves the movement across and within insect tissues. The N-terminal portion of the viral readthrough domain (NRTD) has been implicated as a key determinant of aphid transmission in each of these genera. Here, we report crystal structures of the NRTDs from the poleroviruses turnip yellow virus (TuYV) and potato leafroll virus (PLRV) at 1.53-Å and 2.22-Å resolution, respectively. These adopt a two-domain arrangement with a unique interdigitated topology and form highly conserved dimers that are stabilized by a C-terminal peptide that is critical for proper folding. We demonstrate that the PLRV NRTD can act as an inhibitor of virus transmission and identify NRTD mutant variants that are lethal to aphids. Sequence conservation argues that enamovirus and luteovirus NRTDs will follow the same structural blueprint, which affords a novel approach to block the spread of these agricultural pathogens in a generalizable manner.