Salt-stress and CTD phosphatase-like 4 mediate switching of snRNA to mRNA transcription in Arabidopsis thaliana [CPL4(Oto)]

RNA polymerase II C-terminal domain (CTD) phosphorylation regulates transcription of both protein-coding mRNAs and non-coding RNAs (ncRNAs). However, understanding about CTD-phosphoregulation in plant ncRNA transcription is still obscure. Here we used Arabidopsis CTD phosphatase-like 4 knock-down lines (CPL4RNAi) and show that CPL4 functions in a genome-wide, conditional 3''-extensions of small nuclear RNA (snRNA) and biogenesis of novel snR-DPGs, which are protein-coding snRNA-mRNA fusion transcripts (snR-Downstream Protein-coding Gene). Production of snR-DPG is dependent on pol II snRNA promoter (PIIsnR), and CPL4RNAi promotes readthrough of snRNA 3'-end processing signal and pol II transcription downstream of snRNA. Also discovered was a novel unstable ncRNASSP14, which is driven by a PIIsnR and is conditionally 3''-extended to produce mRNA. In wild type, the snRNA-to-snR-DPG switching is induced by salt stress, and is associated with alteration of CTD phosphorylation status in the transcribing pol II complex. The snR-DPG transcripts occur widely in plants, suggesting that the transcriptional snRNA-to-snR-DPG switching is a previously unknown mechanism ubiquitous in plants to regulate gene expression in response to environmental stresses. Overall design: Examination of two genotypes (wild-type and CPL4 knockdown) in biological triplicate

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Fukudome A, Sun D, Zhang X, Koiwa H