Periodic transcription plays an essential role in eukaryotic cell cycle. We have proposed that a transcription factor (TF) network could function autonomously to drive genome-wide periodic transcription during the cell cycle in budding yeast Saccharomyces cerevisiae. In support of this model, multiple pulses of cell-cycle transcription persist even when budding yeast cells are arrested by perturbing the oscillation of S-phase and mitotic cyclin-dependent kinase (CDK) activity. However, how the dynamics of the TF network are coupled with the normal cell cycle remains unclear. Here we show that G1 cyclin-CDKs and Cdc14 phosphatase oppositely regulate the pulse-generating and pulse-transmitting capability of the TF network during cell cycle commitment and mitotic exit, respectively. Using an integrated genetic-genomic approach, we established that G1 cyclin-CDKs relieve the inhibition of the TF network by inhibiting transcriptional corepressors Whi5/Stb1 and E3 ubiquitin ligase complex APC-Cdh1. Importantly, genetic perturbation of Whi5/Stb1 and APC-Cdh1 in cells lacking G1 cyclin-CDK activity is necessary and sufficient for the TF network to drive a robust pulse of cell-cycle transcription. On the other hand, timely activation of Cdc14 in late mitosis is necessary for preventing ectopic pulses of cell-cycle transcription, potentially through reactivating Whi5/Stb1 and APC-Cdh1 to restore the inhibition of the TF network. In conclusion, we propose that frequency control of periodic transcription in budding yeast is an emergent property of the global network with coupled CDKs and the pulse-generating network.