A glucose-target of rapamycin signaling axis integrates environmental history of heat stress through maintenance of transcription-associated epigenetic memory in Arabidopsis

In nature, plants cope with adversity and have established strategies that recall past episodes and enable them to better cope with stress recurrences by establishing a 'stress memory'. Emerging evidence suggests that glucose (Glc) and target of rapamycin (TOR), central regulators of plant growth, have remarkable functions in stress adaptation. However, whether TOR modulates a stress memory response is so far unknown. Global transcriptome profiling identified that Glc, through TOR, regulates the expression of numerous genes involved in thermomemory. Priming of TOR overexpressors with mild heat showed better stress endurance, whereas TOR RNAi showed reduced thermomemory. This thermomemory is linked with histone methylation at specific sites of heat stress (HS) genes. TOR promotes long-term accumulation of H3K4me3 on thermomemory-associated gene promoters, even when transcription of those genes reverts to their basal level. Our results suggest that ARABIDOPSIS TRITHORAX 1 (ATX1), an H3K4 methyltransferase already shown to regulate H3K4me3 levels at the promoters of HS recovery genes, is a direct target of TOR signaling. The TOR-activating E2Fa binds to the promoter of ATX1 and regulates its expression, which ultimately regulates thermomemory. Collectively, our findings reveal a mechanistic framework in which Glc-TOR signaling determines the integration of stress and energy signaling to regulate thermomemory.

Automated summary

Plants have established a 'stress memory' to better cope with stress recurrences. Glucose and target of rapamycin (TOR) play important roles in stress adaptation. However, the role of TOR in modulating stress memory response is still unknown. This study found that Glucose regulates the expression of genes involved in thermomemory through TOR. Overexpression of TOR resulted in better stress endurance, while TOR RNAi showed reduced thermomemory. Thermomemory is linked with histone methylation at specific sites of heat stress genes. TOR promotes long-term accumulation of H3K4me3 on thermomemory-associated gene promoters. The study also identified TOR-activating E2Fa as a regulator of ATX1 expression, which ultimately regulates thermomemory formation.