INDUCER OF CBF EXPRESSION 1 promotes cold-enhanced immunity by directly activating salicylic acid signaling

Plant Cell. 2024 Jul 2;36(7):2587-2606. doi: 10.1093/plcell/koae096.

Abstract

Cold stress affects plant immune responses, and this process may involve the salicylic acid (SA) signaling pathway. However, the underlying mechanism by which low-temperature signals coordinate with SA signaling to regulate plant immunity remains unclear. Here, we found that low temperatures enhanced the disease resistance of Arabidopsis thaliana against Pseudomonas syringae pv. tomato DC3000. This process required INDUCER OF CBF EXPRESSION 1 (ICE1), the core transcription factor in cold-signal cascades. ICE1 physically interacted with NONEXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1), the master regulator of the SA signaling pathway. Enrichment of ICE1 on the PATHOGENESIS-RELATED GENE 1 (PR1) promoter and its ability to transcriptionally activate PR1 were enhanced by NPR1. Further analyses revealed that cold stress signals cooperate with SA signals to facilitate plant immunity against pathogen attack in an ICE1-dependent manner. Cold treatment promoted interactions of NPR1 and TGACG-BINDING FACTOR 3 (TGA3) with ICE1 and increased the ability of the ICE1-TGA3 complex to transcriptionally activate PR1. Together, our results characterize a critical role of ICE1 as an indispensable regulatory node linking low-temperature-activated and SA-regulated immunity. Understanding this crucial role of ICE1 in coordinating multiple signals associated with immunity broadens our understanding of plant-pathogen interactions.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / immunology
  • Arabidopsis* / metabolism
  • Arabidopsis* / microbiology
  • Basic-Leucine Zipper Transcription Factors / genetics
  • Basic-Leucine Zipper Transcription Factors / metabolism
  • Cold Temperature
  • Disease Resistance / genetics
  • Gene Expression Regulation, Plant*
  • Plant Diseases* / genetics
  • Plant Diseases* / immunology
  • Plant Diseases* / microbiology
  • Plant Immunity* / genetics
  • Promoter Regions, Genetic / genetics
  • Pseudomonas syringae* / pathogenicity
  • Pseudomonas syringae* / physiology
  • Salicylic Acid* / metabolism
  • Signal Transduction*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Salicylic Acid
  • Arabidopsis Proteins
  • ICE1 protein, Arabidopsis
  • NPR1 protein, Arabidopsis
  • Basic-Leucine Zipper Transcription Factors
  • Transcription Factors