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Exons are ligated in an ordered manner without the skipping of exons in the constitutive splicing of pre-mRNAs with multiple introns. To identify factors ensuring ordered exon joining in constitutive pre-mRNA splicing, we previously screened for exon skipping mutants in  Schizosaccharomyces pombe  using a reporter plasmid, and characterized three exon skipping mutants named  ods1  ( o r d ered  s plicing 1),  ods2 , and  ods3 , the responsible genes of which encode Prp2/U2AF 59 , U2AF 23 , and SF1, respectively. They form an SF1-U2AF 59 -U2AF 23  complex involved in recognition of the branch and 3′ splice sites in pre-mRNA. In the present study, we identified a fourth  ods  mutant,  ods4 , which was isolated in an exon-skipping screen. The  ods4   +  gene encodes Cwf16p, which interacts with the  N ine T een  C omplex (NTC), a complex thought to be involved in the first catalytic step of the splicing reaction. We isolated two multi-copy suppressors for the  ods4-1  mutation, Srp2p, an SR protein essential for pre-mRNA splicing, and Tif213p, a translation initiation factor, in  S .  pombe . The overexpression of Srp2p suppressed the exon-skipping phenotype of all  ods  mutants, whereas Tif213p suppressed only  ods4-1 , which has a mutation in the translational start codon of the  cwf16  gene. We also showed that the decrease in the transcriptional elongation rate induced by drug treatment suppressed exon skipping in  ods4-1 . We propose that Cwf16p/NTC participates in the early recognition of the branch and 3′ splice sites and cooperates with the SF1-U2AF 59 -U2AF 23  complex to maintain ordered exon joining.

Cwf16p Associating with the Nineteen Complex Ensures Ordered Exon Joining in Constitutive Pre-mRNA Splicing in Fission Yeast