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. Glc, 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 Glc is largely mediated by HSPs, but the mechanistic basis of this thermotolerance is not well defined. In this study, we show that Glc has a prominent role in providing thermotolerance. Glcmediated thermotolerance involves HSP induction via the TARGET OF RAPAMYCIN (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 HS coincides with TOR-E2Fa expression, substantiating a role for TOR-E2Fa-HLP1 in providing thermotolerance. We also demonstrate that Glc 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 heat stress transcription factor A1s also positively regulate HLP1 transcription, suggesting convergence of the Glc and HS signaling pathways. Loss of functional HLP1 causes HS hypersensitivity, whereas HLP1 overexpressors display increased thermotolerance. HLP1 binds to the promoters of Glc-regulated HS-responsive genes and promotes chromatin acetylation. In addition, Glc modifies the chromatin landscape at thermomemory-related loci by promoting H3K4 trimethylation (H3K4me3). Glc-primed accumulation of H3K4me3 at thermomemory-associated loci is mediated through HLP1. These findings reveal the novel function of Glc-regulated HLP1 in mediating thermotolerance/thermomemory response.

Primary carbohydrate metabolism genes participate in heat stress memory at the shoot apical meristem ofArabidopsis thaliana

“…In addition, we showed that different sets of genes, including FBA6, are involved in generating HS memory in the SAM and cotyledons. To date, only three of the 21 HSFs in Arabidopsis had been shown to participate in HS memory: HSFA1a, HSFA2, and HSFA1e (19,20,29,40). Here, we provide molecular evidence that eight HSFs are likely involved in thermomemory in the SAM.…”

Target of Rapamycin in Control of Autophagy: Puppet Master and Signal Integrator

“…The glc-TOR-E2Fa signaling pathway has also been implicated in thermotolerance and thermomemory [ 157 , 158 ]. Glc-activated TOR phosphorylates E2Fa which binds to the promoter of HLP1 (Hikeshi Like Protein 1), an ortholog of human Hikeshi.…”

“…Glc-activated TOR phosphorylates E2Fa which binds to the promoter of HLP1 (Hikeshi Like Protein 1), an ortholog of human Hikeshi. HLP1 binds to the promoters of many heat response genes and likely activates their expression and thus increases thermotolerance [ 157 ]. Additionally, TOR works in concert with p300 histone acetyltransferase 1 (HAC1) and HLP1 to modulate the chromatin acetylation of heat stress loci and impart short-term acquired thermotolerance.…”

“…Glc-TOR signaling promotes long-term acquired thermotolerance by modifying the chromatin landscape at thermomemory-related loci by promoting H3K4 trimethylation (H3K4me3). Together, these studies show that glc-TOR signaling is important for control of thermotolerance and thermomemory, thus protecting plants from heat stress [ 157 , 158 ]. Recently it has been shown that autophagy negatively regulates thermomemory by selectively targeting heat shock proteins (HSPs) for degradation, and remains highly induced during thermorecovery [ 159 , 160 ].…”

A negative feedback loop of the TOR signaling moderates growth and enables rapid sensing of stress signals in plants

“…TOR phosphorylates E2Fa, which in turn binds to the promoters of target genes to drive their expression 10,40 . To identify the possible role of E2Fa in regulating the expression of FLZ8, we analyzed the presence of the E2Fa binding sites in the promoter region of FLZ8.…”