Pathogen-triggered metabolic adjustments to potato virus Y infection in potato

Potato (Solanum tuberosum L) is affected by several viral pathogens with the most economically damaging being potato virus Y (PVY). At least nine biologically distinct variants of PVY are known to attack potato, with necrotic types named PVY^NTN and PVY^N-Wi being the most recent additions to the list. So far, the molecular plant-virus interactions underlying this pathogenicity are not fully understood. In this study, gas chromatography coupled with mass spectroscopy (GC-MS) was used for an untargeted investigation of the changes in leaf metabolomes of PVY-resistant cultivar Premier Russet, and a susceptible cultivar, Russet Burbank, following inoculation with three PVY strains, PVY^NTN, PVY^N-Wi, and PVY^O. Analysis of the resulting GC-MS spectra with the online software Metaboanalyst (version 5.0) uncovered several common and strain-specific metabolites that are induced by PVY inoculation. In Premier Russet, the major overlap in differential accumulation was found between PVY^N-Wi and PVY^O. However, the 14 significant pathways occurred solely due to PVY^N-Wi. In contrast, the main overlap in differential metabolite profiles and pathways in Russet Burbank was between PVY^NTN and PVY^O. Overall, limited overlap was observed between PVY^NTN and PVY^N-Wi. As a result, PVY^N-Wi-induced necrosis may be mechanistically distinguishable from that of PVY^NTN. Furthermore, 10 common and seven cultivar-specific metabolites as potential indicators of PVY infection and susceptibility/resistance were identified by using PLS-DA and ANOVA. In Russet Burbank, glucose-6-phosphate and fructose-6-phosphate were particularly affected by strain-time interaction. This highlights the relevance of the regulation of carbohydrate metabolism for defense against PVY. Some strain- and cultivar-dependent metabolite changes were also observed, reflecting the known genetic resistance-susceptibility dichotomy between the two cultivars. Consequently, engineering broad-spectrum resistance may be the most effective breeding strategy for managing these necrotic strains of PVY.