# Effector gene silencing coordinated by histone methylation and small RNAs enhances host adaptation in a plant pathogen

## TL;DR

This study shows how a plant pathogen uses two epigenetic strategies together to silence genes that could make it recognizable to host plants, helping it adapt and evade detection.

## Contribution

The study reveals a dual-layered epigenetic mechanism involving H3K27me3 and sRNAs that coordinates effector gene silencing in Phytophthora sojae.

## Key findings

- PsSu(z)12 is a central hub coordinating H3K27me3 and sRNA-mediated silencing of Avr genes.
- 11 out of 12 H3K27me3-regulated effectors are also targeted by sRNAs, showing a strong co-silencing pattern.
- Field isolates show regulatory heterogeneity and plasticity in effector control through epigenetic variation.

## Abstract

Pathogen adaptability driven by epigenetic processes remains poorly understood and poses a significant challenge to sustainable disease management. Histone 3 lysine 27 trimethylation (H3K27me3) and small RNA (sRNA)-mediated silencing of avirulence (Avr) genes are two major strategies that pathogens employ to evade recognition by host resistance (R) proteins. Here, we demonstrate that these two epigenetic mechanisms operate in a coordinated manner to silence Avr genes in the oomycete Phytophthora sojae. CRISPR/Cas9-mediated editing of PsSu(z)12, a core component of the Polycomb repressive complex 2 (PRC2), abolished H3K27me3 deposition at Avr1b and Avr3a, leading to transcriptional reactivation and loss of avirulence. Complementation with PsSu(z)12 restored H3K27me3 and silencing at Avr1b, but not at Avr3a. This prompted sRNA profiling at both loci, revealing differential co-enrichment of sRNA and H3K27me3. Integrated analysis of H3K27me3-enriched chromatin immunoprecipitation, RNA and sRNA sequencing data uncovered a strong locus-specific co-silencing pattern, with 11 out of 12 H3K27me3-regulated arginine-X-leucine-arginine effectors also targeted by sRNAs. Notably, epigenetic variation among field isolates indicated regulatory heterogeneity and plasticity in effector control. Together, our findings establish PsSu(z)12 as a central hub coordinating H3K27me3 and sRNA-mediated effector gene silencing, revealing a dual-layered epigenetic mechanism that enables immune evasion and promotes pathogen adaptation.

Graphical Abstract