An earlier finding that the ecmA and ecmB prestalk cell specific genes exhibited very different responses to cyclic AMP prompted the suggestion that cyclic AMP might act as the major spatial regulator of the prestalk cell developmental pattern in Dictyostelium. A more detailed kinetic analysis in monolayers of Dictyostelium has revealed that cyclic AMP inhibits the rate of expression of all three differentiation inducing factor (DIF) inducible genes, ecmA, ecmB and pDd26. After prolonged incubation, however, cyclic AMP enhances the levels of both ecmA and ecmB mRNAs, and nuclear run-on experiments suggest that cyclic AMP inhibits the degradation of both mRNA species. This complex response to cyclic AMP can explain the differential effects reported previously. Thus depending upon the experimental conditions, cyclic AMP can either enhance or reduce the apparent steady state level of a specific mRNA species. These results are not compatible with the earlier proposal that cyclic AMP is a spatial regulator of the prestalk developmental pattern. Although ecmA and ecmB accumulate rapidly in response to DIF, there is a lag in the accumulation of pD26 mRNA and the induction requires protein synthesis. These results suggest that pDd26 transcription requires the accumulation of an additional factor(s). Inhibition of pDd26 mRNA accumulation by cyclic AMP also occurs during the lag period, suggesting the possibility that cyclic AMP inhibits the accumulation of the, as yet, unknown factor. The inhibitory effect of cyclic AMP on pDd26 gene expression is unaffected by caffeine, suggesting that inhibition does not involve adenylate cyclase activation.(ABSTRACT TRUNCATED AT 250 WORDS)