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Hexokinase1 (HXK1) is an evolutionarily conserved glucose sensor in plants. However, the molecular mechanism through which HXK1 controls the expression of genes encoding proteins involved in photosynthesis is a mystery. Recent research demonstrates that a previously unknown HXK1 nuclear complex controls the expression of specific photosynthetic genes, a process that is independent of glucose metabolism but requires two unexpected partners, VHA-B1 and RPT5B. Both VHA-B1 and RPT5B have well-established and conserved functions in processes that are seemingly unrelated to glucose-dependent regulation of gene expression, and neither of them is a predominantly nuclear protein. Biochemical, genetic, and molecular evidence demonstrates that VHA-B1 and RPT5B directly interact with HXK1 in the nucleus and that the HXK1 complex binds to the cis-acting elements of chlorophyll a/b binding protein 2, a photosynthetic gene that is transcriptionally suppressed by glucose. The identification of the HXK1 nuclear complex reveals an unexpected glucose-signaling mechanism and reinforces the notion that metabolic enzymes can play unique roles in signal transduction by directly controlling gene expression in the nucleus.