TOR represses stress responses through global regulation of H3K27 trimethylation in plants

Abstract

Combinations of epigenetic modifications H3K4me3 and H3K27me3 implicate bistable feature which alternates between on and off state allowing rapid transcriptional changes upon external stimuli. Target of Rapamycin (TOR) functions as a central sensory hub to link a wide range of external stimuli to gene expression. However, the mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remains elusive. Our in silico analysis in Arabidopsis demonstrates that TOR-repressed genes are associated with either bistable or silent chromatin domains. Both domains regulated by TOR signaling pathway are associated with high level of H3K27me3 deposited by CURLY LEAF (CLF) in specific context with LIKE HETEROCHROMATIN PROTEIN1 (LHP1). Chromatin remodeler SWI2/SNF2 ATPase BRAHMA (BRM) activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here we demonstrated both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.

Plant target of rapamycin signaling network: Complexes, conservations, and specificities

“…Most of the genes with the increased DNA methylation are involved in nutrients metabolism (carbon and AAs) and phytohormones signaling transduction processes, which are tightly connected with plant growth and development (Zhu et al, 2020). Moreover, TOR could repress the transcription of stress-related genes by global maintenance of the histone modification at H3K27me3 (Dong et al, 2021). When TOR is active, a high level of H3K27me3 is deposited by curly leaf (CLF), a polycomb group protein (PcG) and major H3K27 tri-methylase in plants (Mozgova and Hennig, 2015) together with like heterochromatin protein1 (LHP1), a CLF cofactor (Wang et al, 2016) in the stress response gene loci.…”

“…Recent studies also revealed that plant TORC1 is involved in stress response by epigenetic DNA modifications and histone modifications (Sharma et al, 2019; Zhu et al, 2020; Dong et al, 2021). Arabidopsis hikeshi‐like protein1 ( At HLP1) binds directly to the promoter of heat shock genes, which leads to histone acetylation and H3K4me3 accumulation to activate and maintain thermo‐memory and high‐temperature tolerance.…”

“…When TOR is active, a high level of H3K27me3 is deposited by curly leaf (CLF), a polycomb group protein (PcG) and major H3K27 tri‐methylase in plants (Mozgova and Hennig, 2015) together with like heterochromatin protein1 (LHP1), a CLF cofactor (Wang et al, 2016) in the stress response gene loci. On the contrary, when TOR is inactive, BRM (switch/sucrose non‐fermentable (SWI/SNF))‐type protein BRAHMA (Torres and Deal, 2019), as an activator of gene expression, restricts CLF activity on the locus of stress‐related genes at bistable chromatin domains (not at the silent chromatin domains) to decrease the levels of H3K27me3 and induce stress‐related genes expression (Figure 4F) (Dong et al, 2021). How TOR modulates CLF/LHP and BRM, and whether there exist other histone modifications regulated by TOR signaling, need to be further investigated.…”