Studies of tomato plants in response to infections with PVX and different PVY isolates reveal a remarkable PVX-PVYNTN synergism and diverse expression profiles of genes involved in different pathways

Abstract

Potato virus Y (PVY) undergoes continuous nucleotide mutation and genome recombination, leading to novel strains with varying pathogenicity on host plants. Little is known about how tomato plants respond to infections with different PVY strains, especially the emerging strains such as PVYNTN and PVYN:O, and in combination with other viral species such as Potato virus X (PVX). In this study, the response of tomato (cultivar Rutgers) plants to single and mixed infections with PVY and PVX was investigated. Plants infected singly with PVYO, PVYN:O, PVYN or PVYNTN developed mosaic symptoms and leaf deformation; whereas plants infected with PVX developed mild local lesion and varying degrees of mosaic and leaf deformation symptoms. Mixed PVX+PVY infections induced more severe symptoms, which include severe local and systemic leaf necrosis, leaf drop and severe leaf deformation, compared to single infections with PVX or PVY, indicating PVX-PVY synergism. The level of PVX-PVY synergism was affected significantly by PVY strains, with PVYNTN being the greatest effector. Quantitative analysis of viral titre indicated that mixed PVX+PVY infections elevated PVX level and reduced PVY level. A comparative transcriptional analysis of 46 key genes involved in signal molecule synthesis and signal transduction using NanoString technology revealed diverse gene expression profiles in both single and mixed infections. Two hierarchical expression clusters, one up-regulated and the other down-regulated, were observed during the infections. In general, mixed infections led to more genes being differentially regulated than single infections. The expression alteration of genes involved in oxidative stress and salicylic acid (SA)-pathways is particularly noteworthy, as the mixed infections, especially PVX+PVYNTN infections, led to a further elevation of reactive oxygen species (ROS) and SA producing abilities and a reduction of ROS scavenging ability over single infections.