HEXOKINASE1 forms a nuclear complex with the PRC2 subunits CURLY LEAF and SWINGER to regulate glucose signaling

The glucose sensor HEXOKINASE1 (HXK1) integrates myriad external and internal signals to regulate gene expression and development in Arabidopsis thaliana. However, how HXK1 mediates glucose signaling in the nucleus remains unclear. Here, using immunoprecipitation-coupled mass spectrometry, we show that two catalytic subunits of Polycomb Repressive Complex 2, SWINGER (SWN) and CURLY LEAF (CLF), directly interact with catalytically active HXK1 and its inactive forms (HXK1(G104D) and HXK1(S177A)) via their evolutionarily conserved SANT domains. HXK1, CLF, and SWN target common glucose-responsive genes to regulate glucose signaling, as revealed by RNA sequencing. The glucose-insensitive phenotypes of the Arabidopsis swn-1 and clf-50 mutants were similar to that of hxk1, and genetic analysis revealed that CLF, SWN, and HXK1 function in the same genetic pathway. Intriguingly, HXK1 is required for CLF- and SWN-mediated histone H3 lysine 27 (H3K27me3) deposition and glucose-mediated gene repression. Moreover, CLF and SWN affect the recruitment of HXK1 to its target chromatin. These findings support a model in which HXK1 and epigenetic modifiers form a nuclear complex to cooperatively mediate glucose signaling, thereby affecting the histone modification and expression of glucose-regulated genes in plants.

Automated summary

This study reveals that the glucose sensor HXK1 interacts with Polycomb Repressive Complex 2 subunits SWN and CLF to regulate glucose signaling in Arabidopsis thaliana. They target glucose-responsive genes and function in the same genetic pathway. HXK1 is also involved in histone modification and gene repression, and CLF and SWN affect the recruitment of HXK1 to chromatin.