Phosphorylation at the carboxy-terminal domain of the largest subunit of RNA polymerase II plays a critical role in transcription, and histone acetylation is correlated with active transcription. However, the regulatory mechanisms by which histone acetylation modulates RNA polymerase II phosphorylation in plants remain unclear. Here we show that two functionally redundant bromodomain-containing proteins, global transcription factor group E2 (GTE2) and GTE7, can bind to acetylated histone H4. Both GTE2 and GTE7 interact with cyclin-dependent kinase-like 9 (CDKL9), which belongs to a plant-specific CDKL group. Unlike canonical CDKs, CDKL9 functions in a cyclin- and CDK-activating-kinase-independent manner and can phosphorylate at least the serine 2 and serine 5 residues of the carboxy-terminal domain in vitro. The GTE2/GTE7-CDKL9 complex is required to maintain serine 2 and serine 5 phosphorylation under heat stress. Consistently, loss-of-function gte2/gte7 and cdkl9 mutants show similar heat-sensitive phenotypes. We also demonstrate that the acetylated-histone-binding activity of GTE7 is essential for the association of CDKL9 with chromatin and for plant heat tolerance. Together, these findings provide mechanistic insight into transcriptional regulation via histone acetylation in response to heat stress and suggest that plants might have evolved a unique group of carboxy-terminal domain kinases for stress tolerance.