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Alternative polyadenylation (APA) is widespread in neuronal development and activity-mediated neural plasticity. However, the underlying molecular mechanisms are largely unknown. We used systematic genetic studies and genome-wide surveys of the transcriptional landscape to identify a context-dependent regulatory pathway controlling APA in the  Caenorhabditis elegans  nervous system. Loss of function in  ssup-72 , a Ser5 phosphatase for the RNA polymerase II (Pol II) C-terminal domain (CTD), dampens transcription termination at a strong intronic polyadenylation site (PAS) in  unc-44/ankyrin  yet promotes termination at the weak intronic PAS of the MAP kinase  dlk-1.  A nuclear protein, SYDN-1, which regulates neuronal development, antagonizes the function of SSUP-72 and several nuclear polyadenylation factors. This regulatory pathway allows the production of a neuron-specific isoform of  unc-44  and an inhibitory isoform of  dlk-1 . Dysregulation of the  unc-44  and  dlk-1  mRNA isoforms in  sydn-1  mutants impairs neuronal development. Deleting the intronic PAS of  unc-44  results in increased pre-mRNA processing of neuronal ankyrin and suppresses  sydn-1  mutants. These results reveal a mechanism by which regulation of CTD phosphorylation controls coding region APA in the nervous system.

Context-dependent modulation of Pol II CTD phosphatase SSUP-72 regulates alternative polyadenylation in neuronal development