During fruiting body morphogenesis in Myxococcus xanthus, the intercellular C-signal induces aggregation, sporulation and developmental gene expression. To understand how a single signal system may induce temporally separated processes, we have focused on the class II gene, which codes for an essential component in the C-signal transduction pathway. We report that class II is identical to fruA and codes for a DNA binding response regulator. Transcription of fruA is developmentally regulated and depends on the early acting intercellular A- and E-signals. However, fruA transcription is independent of C-signal. Rather, genetic evidence suggests that C-signal controls FruA activity post-translationally. Genetic evidence strongly indicates that FruA is activated by phosphorylation. We propose that C-signalling results in the phosphorylation of FruA, thus activating FruA to interact with downstream targets. In the motility branch of the C-signalling pathway, FruA interacts with the Frz motility system; in the sporulation branch, we show that FruA is required for transcription of the sporulation locus devRS. On the basis of the two levels of control of FruA activity, we propose that FruA serves as a control point for the temporal co-ordination of intercellular signals during M. xanthus development.