The StPti5 ethylene response factor acts as a susceptibility factor by negatively regulating the potato immune response to pathogens

New Phytol. 2024 Oct;244(1):202-218. doi: 10.1111/nph.20004. Epub 2024 Aug 11.

Abstract

Ethylene response factors (ERFs) have been associated with biotic stress in Arabidopsis, while their function in non-model plants is still poorly understood. Here we investigated the role of potato ERF StPti5 in plant immunity. We show that StPti5 acts as a susceptibility factor. It negatively regulates potato immunity against potato virus Y and Ralstonia solanacearum, pathogens with completely different modes of action, and thereby has a different role than its orthologue in tomato. Remarkably, StPti5 is destabilised in healthy plants via the autophagy pathway and accumulates exclusively in the nucleus upon infection. We demonstrate that StEIN3 and StEIL1 directly bind the StPti5 promoter and activate its expression, while synergistic activity of the ethylene and salicylic acid pathways is required for regulated StPti expression. To gain further insight into the mode of StPti5 action in attenuating potato defence responses, we investigated transcriptional changes in salicylic acid deficient potato lines with silenced StPti5 expression. We show that StPti5 regulates the expression of other ERFs and downregulates the ubiquitin-proteasome pathway as well as several proteases involved in directed proteolysis. This study adds a novel element to the complex puzzle of immune regulation, by deciphering a two-level regulation of ERF transcription factor activity in response to pathogens.

Keywords: Ralstonia solanacearum; Pti5; Solanum tuberosum (potato); ethylene response factor; immune signalling; potato virus Y (PVY); susceptibility factor.

MeSH terms

  • Autophagy
  • Cell Nucleus / metabolism
  • Ethylenes* / metabolism
  • Gene Expression Regulation, Plant*
  • Plant Diseases* / immunology
  • Plant Diseases* / microbiology
  • Plant Diseases* / virology
  • Plant Immunity*
  • Plant Proteins* / genetics
  • Plant Proteins* / metabolism
  • Potyvirus* / physiology
  • Promoter Regions, Genetic* / genetics
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding
  • Ralstonia solanacearum* / physiology
  • Salicylic Acid* / metabolism
  • Solanum tuberosum* / genetics
  • Solanum tuberosum* / immunology
  • Solanum tuberosum* / microbiology
  • Solanum tuberosum* / virology

Substances

  • Plant Proteins
  • Ethylenes
  • Salicylic Acid
  • ethylene
  • Proteasome Endopeptidase Complex