Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL-INDUCED CELL DEATH1

New Phytol. 2018 Oct;220(1):232-248. doi: 10.1111/nph.15277.

Abstract

The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL-INDUCED CELL DEATH1 (RCD1). We use pathogen infection assays as well as molecular and biochemical analyses to test the hypothesis that HaRxL106 manipulates RCD1 to attenuate transcriptional activation of defense genes. We report that HaRxL106 suppresses transcriptional activation of salicylic acid (SA)-induced defense genes and alters plant growth responses to light. HaRxL106-mediated suppression of immunity is abolished in RCD1 loss-of-function mutants. We report that RCD1-type proteins are phosphorylated, and we identified Mut9-like kinases (MLKs), which function as phosphoregulatory nodes at the level of photoreceptors, as RCD1-interacting proteins. An mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared with wild-type plants, suggesting that MLKs also affect transcriptional regulation of SA signaling. Based on the combined evidence, we hypothesize that nuclear RCD1/MLK complexes act as signaling nodes that integrate information from environmental cues and pathogen sensors, and that the Arabidopsis downy mildew pathogen targets RCD1 to prevent activation of plant immunity.

Keywords: Arabidopsis thaliana; Hyaloperonospora arabidopsidis; RADICAL-INDUCED CELL DEATH1; oomycete pathogen; pathogen effector; plant innate immunity; salicylic acid (SA).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP Ribose Transferases / metabolism
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / immunology*
  • Arabidopsis / microbiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Gene Expression Regulation, Plant / radiation effects
  • Mutation / genetics
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Oomycetes / drug effects
  • Oomycetes / isolation & purification
  • Oomycetes / metabolism*
  • Oomycetes / pathogenicity
  • Plant Diseases / microbiology
  • Plant Immunity* / drug effects
  • Plants, Genetically Modified
  • Protein Domains
  • Protein Multimerization / drug effects
  • Proteins / metabolism*
  • Salicylic Acid / pharmacology
  • Signal Transduction / radiation effects
  • Transcription, Genetic / drug effects
  • Virulence / drug effects

Substances

  • Arabidopsis Proteins
  • NPR1 protein, Arabidopsis
  • Nuclear Proteins
  • Proteins
  • RCD1 protein, Arabidopsis
  • ADP Ribose Transferases
  • Salicylic Acid