Transcription commonly occurs in bursts resulting from alternating productive (ON) and quiescent (OFF) periods. Yet how transcriptional bursts are regulated to determine spatiotemporal transcriptional activity remains unclear. Here we perform live transcription imaging of key developmental genes in the fly embryo, with single polymerase sensitivity. Quantification of single allele transcription rates and multi-polymerase bursts reveals shared bursting relationships among all genes, across time and space, as well as cis-and trans-perturbations. We identify the allele's ON-probability as the main determinant of the transcription rate, while changes in the transcription initiation rate are limited. Any given ON-probability determines a specific combination of mean ON and OFF times, preserving a constant characteristic bursting time scale. Our findings point to a convergence of various regulatory processes that predominantly affect the ON-probability, thereby controlling mRNA production rather than mechanism-specific modulation of ON and OFF times. Our results thus motivate and guide new investigations into the mechanisms implementing these bursting rules and governing transcriptional regulation.