In Escherichia coli synthesis of glucosamine-6-phosphate synthase GlmS is feedback-controlled by a regulatory cascade composed of small RNAs GlmY and GlmZ. When GlcN6P becomes limiting, GlmY accumulates and inhibits processing of GlmZ. Full-length GlmZ base-pairs with the glmS transcript and activates synthesis of GlmS, which re-synthesizes GlcN6P. Here we show that glmY expression is controlled by two overlapping promoters with the same transcription start site. A sigma(70)-dependent promoter contributes to glmY transcription during exponential growth. Alternatively, glmY can be transcribed from a sigma(54)-dependent promoter, which requires the YfhK/YfhA two-component system for activity. YfhK is a sensor kinase and YfhA is a response regulator that contains a sigma(54) interaction domain. YfhA binds to a DNA region located more than 100 bp upstream of glmY. Three copies of the conserved sequence TGTCN(10)GACA contribute to binding, and the two sites next to glmY are essential for activation of the sigma(54)-dependent promoter by YfhA. YfhK and YfhA upregulate GlmY when cells enter the stationary growth phase, whereas regulation by glucosamine-6-phosphate occurs post GlmY transcription. Target genes regulated by YfhK and YfhA were unknown so far. We propose to rename these proteins to GlrK and GlrR, for glmY regulating kinase and response regulator respectively.