Insights in luteovirid structural biology guided by chemical cross-linking and high resolution mass spectrometry

Authors: ALEXANDER, MARIKO - Cornell University; MOHR, JARED - University Of Washington; Deblasio, Stacy; CHAVEZ, JUAN - University Of Washington; ZIEGLER-GRAFF, VERONIQUE - Université De Strasbourg: Accueil; BRAULT, VERONIQUE - Inra- Site D'Orleans Unite De Zoologie Forestiere; BRUCE, JAMES - University Of Washington; Heck, Michelle

Submitted to: Virus Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/9/2017
Publication Date: 5/11/2017
Citation: Alexander, M., Mohr, J.P., DeBlasio, S.L., Chavez, J., Ziegler-Graff, V., Brault, V., Bruce, J., Heck, M.L. 2017. Insights in luteovirid structural biology guided by chemical cross-linking and high resolution mass spectrometry. Virus Research. 241:42-52. https://doi.org/10.1016/j.virusres.2017.05.005.
DOI: https://doi.org/10.1016/j.virusres.2017.05.005

Interpretive Summary: Turnip yellows virus (TuYV), a virus in the family Luteoviridae, is an economically important pathogen of canola and other Brassicaceae. TuYV and similar viruses are transmitted among plants by aphids, small plant-infesting insects that feed on the plant sap. Like other related viruses in the Luteoviridae, TuYV is transported in both aphid vectors and plant hosts as virions. Virions contain the infectious viral genome and are encased in a protective cage made up of viral proteins. The 3-D shape of these proteins are critical to determine how the virus is transmitted by insects and how it infects plants. Using two techniques called protein cross-linking and mass spectrometry, the 3-D shape of the TuYV virion was predicted and compared to other, related viruses. This comparison enabled us to identify regions in both viruses which are critical for virion stability and infectivity. The protein cross-linking approach also enabled us to identify an interaction between the virion and another viral protein, P1, whose function is to cleave proteins. We hypothesize that the interaction between P1 and the virion may regulate the final shape and function of a virion protein. This new information is critical to develop precision virus management strategies that block aphid transmission and host plant infection.

Technical Abstract: Interactions among plant pathogenic viruses in the family /react-text Luteoviridae react-text: 233 and their plant hosts and insect vectors are governed by the topology of the viral capsid, which is the sole vehicle for long distance movement of the viral genome. Previous application of a mass spectrometry-compatible cross-linker to preparations of the luteovirid /react-text Potato leafroll virus react-text: 235 (PLRV; /react-text Luteoviridae react-text: 237 : /react-text Polerovirus react-text: 239 ) revealed a detailed network of interactions between viral structural proteins and enabled generation of the first cross-linking guided coat protein models. In this study, we extended application of chemical cross-linking technology to the related /react-text Turnip yellows virus react-text: 241 (TuYV; /react-text Luteoviridae react-text: 243 : /react-text Polerovirus react-text: 245 ). Remarkably, all cross-links found between sites in the viral coat protein found for TuYV were also found in PLRV. Guided by these data, we present two models for the TuYV coat protein trimer, the basic structural unit of luteovirid virions. Additional cross-links found between the TuYV coat protein and a site in the viral protease domain suggest a possible role for the luteovirid protease in regulating the structural biology of these viruses.