Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato

J Exp Bot. 2014 Mar;65(4):1095-109. doi: 10.1093/jxb/ert447. Epub 2014 Jan 13.

Abstract

The purpose of the study was to investigate the role of salicylic acid (SA) signalling in Ny-1-mediated hypersensitive resistance (HR) of potato (Solanum tuberosum L.) to Potato virus Y (PVY). The responses of the Ny-1 allele in the Rywal potato cultivar and transgenic NahG-Rywal potato plants that do not accumulate SA were characterized at the cytological, biochemical, transcriptome, and proteome levels. Analysis of noninoculated and inoculated leaves revealed that HR lesions started to develop from 3 d post inoculation and completely restricted the virus spread. At the cytological level, features of programmed cell death in combination with reactive oxygen species burst were observed. In response to PVY infection, SA was synthesized de novo. The lack of SA accumulation in the NahG plants led to the disease phenotype due to unrestricted viral spreading. Grafting experiments show that SA has a critical role in the inhibition of PVY spreading in parenchymal tissue, but not in vascular veins. The whole transcriptome analysis confirmed the central role of SA in orchestrating Ny-1-mediated responses and showed that the absence of SA leads to significant changes at the transcriptome level, including a delay in activation of expression of genes known to participate in defence responses. Moreover, perturbations in the expression of hormonal signalling genes were detected, shown as a switch from SA to jasmonic acid/ethylene signalling. Viral multiplication in the NahG plants was accompanied by downregulation of photosynthesis genes and activation of multiple energy-producing pathways.

Keywords: Plant–pathogen interactions; Potato virus Y; Potyviridae; Solanum tuberosum; salicylic acid; whole transcriptome analysis..

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis
  • Cyclopentanes / metabolism
  • Down-Regulation
  • Energy Metabolism
  • Ethylenes / metabolism
  • Gene Expression Regulation, Plant
  • Host-Pathogen Interactions
  • Oxylipins / metabolism
  • Photosynthesis
  • Plant Diseases / immunology*
  • Plant Diseases / virology
  • Plant Growth Regulators / metabolism
  • Plant Immunity
  • Plant Leaves / genetics
  • Plant Leaves / immunology
  • Plant Leaves / virology
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Potyvirus / physiology*
  • Reactive Oxygen Species / metabolism
  • Salicylic Acid / metabolism*
  • Signal Transduction
  • Solanum tuberosum / genetics*
  • Solanum tuberosum / immunology
  • Solanum tuberosum / virology
  • Transcriptome*

Substances

  • Cyclopentanes
  • Ethylenes
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • Reactive Oxygen Species
  • jasmonic acid
  • ethylene
  • Salicylic Acid