The Arabidopsis PHD-finger protein EDM2 has multiple roles in balancing NLR immune receptor gene expression

Abstract

Plant NLR-type receptors serve as sensitive triggers of host immunity. Their expression has to be well-balanced, due to their interference with various cellular processes and dosedependency of their defense-inducing activity. A genetic "arms race" with fast-evolving pathogenic microbes requires plants to constantly innovate their NLR repertoires. We previously showed that insertion of the COPIA-R7 retrotransposon into RPP7 co-opted the epigenetic transposon silencing signal H3K9me2 to a new function promoting expression of this Arabidopsis thaliana NLR gene. Recruitment of the histone binding protein EDM2 to COPIA-R7associated H3K9me2 is required for optimal expression of RPP7. By profiling of genomewide effects of EDM2, we now uncovered additional examples illustrating effects of transposons on NLR gene expression, strongly suggesting that these mobile elements can play critical roles in the rapid evolution of plant NLR genes by providing the "raw material" for gene expression mechanisms. We further found EDM2 to have a global role in NLR expression control. Besides serving as a positive regulator of RPP7 and a small number of other NLR genes, EDM2 acts as a suppressor of a multitude of additional NLR genes. We speculate that the dual functionality of EDM2 in NLR expression control arose from the need to compensate for fitness penalties caused by high expression of some NLR genes by suppression of others. Moreover, we are providing new insights into functional relationships of EDM2 with its interaction partner, the RNA binding protein EDM3/AIPP1, and its target gene IBM1, encoding an H3K9-demethylase.

Genome‐wide distribution and functions of the AAE complex in epigenetic regulation in Arabidopsis

“…In addition, a substantial number of ASI1 and EDM2 ChIP peaks were mapped to intergenic TEs (Figure 1B). EDM2 has been shown to be involved in the regulation of some chromosomal arms‐ and pericentromeric regions‐located TEs (Tsuchiya and Eulgem, 2013b; Lai et al, 2020). To examine whether the AAE complex has a function in the regions not corresponding to TE‐overlapping genes, we selected representative loci to evaluate their chromatin status and gene expression in different genotypes.…”

CREB-binding protein gene,HAC701, negatively regulates WRKY45-dependent immunity in rice

“…This compensation functionality has been shown in a PHD-finger protein, Enhanced Downy Mildew 2 (EDM2), in NLR (i.e. a type of R protein) protein expression control as it affects plant fitness (60). Therefore, it is also likely that the expression regulation of WRKY45 locus as well as the decoys/sensors may be subjected to compensatory regulation in the case of HAC701 mutation.…”

A Meta-Analysis Reveals Opposite Effects of Biotic and Abiotic Stresses on Transcript Levels of Arabidopsis Intracellular Immune Receptor Genes

“…Expression suppression of some NLR genes may occur simultaneously with expression increase of other NLR genes in order to prevent overactivation of immune responses and its consequent fitness costs. For example, an immunity regulator ENHANCED DOWNY MILDEW 2 (EDM2) positively regulates expression of RECOGNITION OF PERONOSPORA PARASITICA 7 ( RPP7 ) and a small number of other NLR genes, whereas it represses the expression of a number of other NLR genes (Lai et al, 2020 ). Studying the molecular mechanism and biological relevance of NLR genes that are often repressed by pathogens in the context of plant–microbe interaction is expected to bring a new insight into NLR function.…”