Hexokinase 1 facilitates post-germinative seedling growth through its catalytic function

In darkness or dim light PHYTOCHROME INTERACTING FACTORS (PIFs) induce skotomorphogenic seedling growth, which is exemplified by elongated hypocotyls. Likewise, HEXOKINASE1 (HXK1) has been reported to promote hypocotyl growth under light and nutrient limiting conditions. HXK1 is known to operate as a glucose-phosphorylating enzyme and as a glucose activated sensor-signalling molecule. Earlier work implicated HXK1 sensor-signalling in hypocotyl elongation; however, less is known of whether HXK1 enzymatic function and/or HXK1-PIF pathway interaction are involved. We provide genetic evidence that HXK1-mediated glucose-phosphorylation is required for hypocotyl cell expansion in light limiting conditions. Application of glucose-6-phosphate, the HXK1 enzymatic product, restores short gin2-1/hxk1-3 hypocotyls to wild-type length. Further, components of nuclear-located HXK1 sensor-signalling complexes, comprising VHA-B1 and RPT5B, or the Polycomb Repressive Complex 2 subunits SWN and CLF, do not contribute to this response. Unlike gin2-1/hxk1-3, the vha-B1, rpt5b swn-7, clf28, clf29 alleles only disrupt hypocotyl growth following the application of exogenous glucose and not in control conditions. mRNA-seq analysis illustrates that HXK1 and PIF signalling intersect at genes with known roles in light signalling. HXK1 imposes strong negative regulation on chloroplast and mitochondrial genomes, and also branched-chain amino acid catabolism pathway genes, which can provide a source of respiratory substrates in starvation conditions. Our study establishes the importance of HXK1 enzymatic function in supporting hypocotyl cell expansion, amino acid metabolism and the transcriptional regulation of light signalling genes.