U small nuclear RNAs (snRNAs) and mRNAs are both transcribed by RNA polymerase II (Pol II), but the snRNAs have unusual TATA-less promoters and are neither spliced nor polyadenylated; instead, 3 processing is directed by a highly conserved 3 end formation signal that requires initiation from an snRNA promoter. Here we show that the C-terminal domain (CTD) of Pol II is required for efficient U2 snRNA transcription, as it is for mRNA transcription. However, CTD kinase inhibitors, such as 5,6-dichloro-1--D-ribofuranosylbenzimidazole (DRB) and 1-(5-isoquinolinesulfonyl)-2-methylpiperazine (H7), that block mRNA elongation do not affect U2 transcription, although 3 processing of the U2 primary transcript is impaired. We show further that U2 transcription is preferentially inhibited by low doses of UV irradiation or actinomycin D, which induce CTD kinase activity, and that UV inhibition can be rescued by treatment with DRB or H7. We propose that Pol II complexes transcribing snRNAs and mRNAs have distinct CTD phosphorylation patterns. mRNA promoters recruit factors including kinases that hyperphosphorylate the CTD, and the CTD in turn recruits proteins needed for mRNA splicing and polyadenylation. We predict that snRNA promoters recruit factors including a CTD kinase(s) whose snRNA-specific phosphorylation pattern recruits factors required for promoter-coupled 3 end formation.RNAs that encode proteins are transcribed by RNA polymerase II (Pol II) in almost all eukaryotes. In contrast, untranslated RNAs are transcribed by all three RNA polymerases: 5.8, 18, and 28S rRNA by Pol I; 5S rRNA, tRNA, and U6 small nuclear RNA (snRNA) by Pol III (56); and the other U snRNAs, which function in mRNA splicing and various RNA processing events, by Pol II (27). Kinetoplastid protozoa, a class of early diverging eukaryotes, are exceptions to these rules. Kinetoplastid snRNAs are transcribed not by Pol II but by Pol III (65), and certain mRNAs, including the immunologically important variant surface glycoprotein message, are hybrids of a U snRNA-like spliced leader transcribed by Pol II and a protein-coding mRNA body transcribed by Pol I (19).Although U snRNAs and mRNAs are both transcribed by Pol II in mammals, the genes are very different. U snRNA promoters have no TATA box and rely instead upon a dedicated U snRNA-specific promoter consisting of a highly conserved proximal sequence element (PSE) and an enhancer-like distal sequence element spaced one nucleosome apart (27). In addition, U snRNA genes are short (typically only a few hundred base pairs) and lack introns, whereas genes encoding mRNAs can span megabases and usually contain many introns. Also, U snRNA genes are typically present in multiple copies in higher eukaryotes-the human U1 and U2 genes are tandemly repeated (6, 40, 66, 68)-whereas most protein-coding genes are present in only one or a few copies per haploid genome.U snRNA processing also differs from mRNA processing. U snRNAs are neither spliced nor polyadenylated; instead, formation of the first U snRNA interme...