Polycomb Repressive Complex 2 and KRYPTONITE regulate pathogen-induced programmed cell death in Arabidopsis

Abstract

The Polycomb Repressive Complex 2 (PRC2) is well-known for its role in controlling developmental transitions by suppressing the premature expression of key developmental regulators. Previous work revealed that PRC2 also controls the onset of senescence, a form of developmental programmed cell death (PCD) in plants. Whether the induction of PCD in response to stress is similarly suppressed by the PRC2 remained largely unknown. In this study, we explored whether PCD triggered in response to immunity- and disease-promoting pathogen effectors is associated with changes in the distribution of the PRC2-mediated histone H3 lysine 27 trimethylation (H3K27me3) modification in Arabidopsis thaliana. We furthermore tested the distribution of the heterochromatic histone mark H3K9me2, which is established, to a large extent, by the H3K9 methyltransferase KRYPTONITE, and occupies chromatin regions generally not targeted by PRC2. We report that effector-induced PCD caused major changes in the distribution of both repressive epigenetic modifications and that both modifications have a regulatory role and impact on the onset of PCD during pathogen infection. Our work highlights that the transition to pathogen-induced PCD is epigenetically controlled, revealing striking similarities to developmental PCD.

Dynamics of H3K27me3 Modification on Plant Adaptation to Environmental Cues

“…Consistently, MEA-overexpressing transgenic plants are susceptible to fungal pathogens, bacterial pathogens, and Pst-AvrRpt2, whereas mea-6 mutant plants are more resistant to bacterial pathogens [156,183]. Moreover, loss of SWN caused a significantly increased hypersensitive response (HR) during the time course of AvrRpt2 induction, revealing a role of SWN in attenuating PCD [224]. In rice, the H3K27me3 demethylase, OsJMJ705, could be induced by stress signals and pathogen infection.…”

“…PTI and ETI result in many overlapping downstream outputs, such as reactive oxygen species (ROS) burst, programmed cell death (PCD), transcriptional reprograming, and phytohormone signaling (e.g., salicylic acid (SA) and jasmonate acid (JA)) [221]. Besides, genome-wide H3K27me3 atlas was observed in plant responses to infection by pathogens [219,220,[222][223][224]. The expression of MEA could be induced by either pathogen inoculation or exogenous application of JA or SA.…”

Zebularine induces enzymatic DNA–protein crosslinks in 45S rDNA heterochromatin of Arabidopsis nuclei

“…For native chromatin immunoprecipitation (N-ChIP), 5-day-old seedlings were incubated in mock and 40 μM zebularine for 24 h. About 250 seedlings from two independent biological replicates were frozen in liquid nitrogen and were used for crude nuclei extraction for ChIP experiments as previously described without crosslinking with formaldehyde ( 43 , 44 ). Antibody against RFP raised in rabbit (600-401-379, Rockland Antibodies & Assays) was used for ChIP.…”

Transcriptional regulation of plant innate immunity

“…Chromatin remodeling also plays a role during ETI-triggered PCD. During this process chromocenters (regions with heterochromatin) get less dense and different chromatin marks get redistributed, such as the repressive marks H3K9me2 and H3K27me3, leading to altered transcription [ 82 ]. Studies with chromatin remodeling mutants suggest that this remodeling mostly attenuates PCD, possibly to prevent it from happening too rapidly or at the wrong time [ 82 ].…”