Reciprocal control of metabolic and chromatin regulators improves rice tolerance to heat

Plant metabolic activities are regulated to adapt to the fluctuating environment for optimized growth, while interplay between metabolic and chromatin pathways plays an essential role in environmental adaptation. However, how metabolic and chromatin regulators cooperate to control metabolite accumulation and gene expression required for stress tolerance remains unclear. Here, we show that the pyruvate kinase 1 (PK1) has a function to integrate stress signals for metabolic and epigenetic controls of heat tolerance in rice. Over-expression of PK1 enhances plant tolerance to heat, while its loss-of-function decreases the recovery rate from heat stress. Heat stress induces PK1 production, nuclear enrichment, lysine acetylation and activity for pyruvate accumulation, H3T11 phosphorylation (H3T11p) and H3K9 acetylation (H3K9ac), and gene expression. In addition, PK1 phosphorylates General control non-repressed protein 5 (GCN5) and stimulates its activity for H3K9ac. Conversely, under heat stress GCN5 enhances PK1 lysine acetylation and enhances its activity for H3T11p and pyruvate production. The PK1 and GCN5-controlled H3T11p and H3K9ac are required for heat stress-responsive gene expression. These results establish PK1 as key player linking metabolic and chromatin pathways and uncover a mutually stimulating mechanism between metabolic and chromatin regulators for stress tolerance in rice.