Glucose-regulated HLP1 acts as a key molecule in governing thermomemory

Abstract

Induction of heat shock proteins (HSPs) in response to heat stress (HS) is indispensable for conferring thermotolerance. Glucose, a fundamental signaling and metabolic molecule, provides energy to stressed seedlings to combat stress. The recovery of stressed plants from detrimental HS in response to glucose is largely mediated by HSPs, but the mechanistic basis of this thermotolerance is not well defined. In this study, we show that glucose has a prominent role in providing thermotolerance. Glucose-mediated thermotolerance involves HSP induction via the TOR-E2Fa signaling module. Apart from HSPs, TOR-E2Fa also regulates the Arabidopsis (Arabidopsis thaliana) ortholog of human Hikeshi, named HIKESHI-LIKE PROTEIN1 (HLP1). Expression of proHLP1::GUS in the shoot apical meristem (SAM) after heat stress coincides with TOR-E2Fa expression, substantiating a role for TOR-E2Fa-HLP1 in providing thermotolerance. We also demonstrate that glucose along with heat could induce proliferation activity in the SAM after HS recovery, which was arrested by the TOR inhibitor AZD-8055. Molecular and physiological studies suggest that HS-activated HSFA1s also positively regulate HLP1 transcription, suggesting convergence of the glucose and HS signaling pathways. Loss of functional HLP1 causes HS hypersensitivity, while HLP1 overexpressors (OEs) display increased thermotolerance. HLP1 binds to the promoters of glucose-regulated HS responsive genes and promotes chromatin acetylation. In addition, glucose modifies the chromatin landscape at thermomemory-related loci by promoting H3K4 trimethylation (H3K4me3). Glucose-primed accumulation of H3K4me3 at thermomemory-associated loci is mediated through HLP1. These findings reveal the novel function of glucose-regulated HLP1 in mediating thermotolerance/thermomemory response.