Two adjacent NLR genes conferring quantitative resistance to clubroot disease in Arabidopsis are regulated by a stably inherited epiallelic variation

Plant Commun. 2024 May 13;5(5):100824. doi: 10.1016/j.xplc.2024.100824. Epub 2024 Jan 23.

Abstract

Clubroot caused by the protist Plasmodiophora brassicae is a major disease affecting cultivated Brassicaceae. Using a combination of quantitative trait locus (QTL) fine mapping, CRISPR-Cas9 validation, and extensive analyses of DNA sequence and methylation patterns, we revealed that the two adjacent neighboring NLR (nucleotide-binding and leucine-rich repeat) genes AT5G47260 and AT5G47280 cooperate in controlling broad-spectrum quantitative partial resistance to the root pathogen P. brassicae in Arabidopsis and that they are epigenetically regulated. The variation in DNA methylation is not associated with any nucleotide variation or any transposable element presence/absence variants and is stably inherited. Variations in DNA methylation at the Pb-At5.2 QTL are widespread across Arabidopsis accessions and correlate negatively with variations in expression of the two genes. Our study demonstrates that natural, stable, and transgenerationally inherited epigenetic variations can play an important role in shaping resistance to plant pathogens by modulating the expression of immune receptors.

Keywords: ADR1-L3; AT5G47260; AT5G47280; Plasmodiophora brassicae; clubroot; ddm1; methylation.

MeSH terms

  • Alleles
  • Arabidopsis Proteins / genetics
  • Arabidopsis* / genetics
  • Arabidopsis* / immunology
  • DNA Methylation
  • Disease Resistance* / genetics
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • NLR Proteins / genetics
  • NLR Proteins / metabolism
  • Plant Diseases* / genetics
  • Plant Diseases* / immunology
  • Plant Diseases* / parasitology
  • Plasmodiophorida / physiology
  • Quantitative Trait Loci / genetics