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 t...

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Bibliographic Details
Published in:Journal of integrative plant biology 2022-06, Vol.64 (6), p.1168-1180
Main Authors: Liu, Yutong, Bai, Yunshu, Li, Ning, Li, Mengting, Liu, Wenxin, Yun, Dae‐Jin, Liu, Bao, Xu, Zheng‐Yi
Format: Article
Language:English
Subjects:
Arabidopsis thaliana
Catalytic subunits
Chromatin
Epigenetics
Gene expression
Gene sequencing
Genes
Genetic analysis
Glucose
glucose sensor
hexokinase
Histone H3
histone methylation
Histones
Immunoprecipitation
Leaves
Lysine
Mass spectrometry
Mass spectroscopy
Phenotypes
Polycomb group proteins
Signaling
transcriptional regulation
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Summary: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 (HXK1G104D and HXK1S177A) 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. The glucose sensor HEXOKINASE1 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.
ISSN:1672-9072
1744-7909
DOI:10.1111/jipb.13261