title: Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals.
abstract: Ribonuclease P (RNase P) is an essential enzyme required for 5'-maturation of tRNA. While an RNA-free, protein-based form of RNase P exists in eukaryotes, the ribonucleoprotein (RNP) form is found in all domains of life. The catalytic component of the RNP is an RNA known as RNase P RNA (RPR). Eukaryotic RPR genes are typically transcribed by RNA polymerase III (pol III). Here we showed that the RPR gene in Drosophila, which is annotated in the intron of a pol II-transcribed protein-coding gene, lacks signals for transcription by pol III. Using reporter gene constructs that include the RPR-coding intron from Drosophila, we found that the intron contains all the sequences necessary for production of mature RPR but is dependent on the promoter of the recipient gene for expression. We also demonstrated that the intron-coded RPR copurifies with RNase P and is required for its activity. Analysis of RPR genes in various animal genomes revealed a striking divide in the animal kingdom that separates insects and crustaceans into a single group in which RPR genes lack signals for independent transcription and are embedded in different protein-coding genes. Our findings provide evidence for a genetic event that occurred approximately 500 million years ago in the arthropod lineage, which switched the control of the transcription of RPR from pol III to pol II.
authors.affiliation: Molecular Cellular Developmental Biology Program, Ohio State University, Columbus, Ohio, United States of America; Department of Molecular Genetics, Ohio State University, Columbus, Ohio, United States of America.
authors.forename: Sathiya N
authors.initials: SN
authors.lastname: Manivannan
authors.affiliation: Department of Chemistry and Biochemistry, Ohio State University, Columbus, Ohio, United States of America; Center for RNA Biology, Ohio State University, Columbus, Ohio, United States of America.
authors.forename: Lien B
authors.initials: LB
authors.lastname: Lai
authors.affiliation: Molecular Cellular Developmental Biology Program, Ohio State University, Columbus, Ohio, United States of America; Department of Chemistry and Biochemistry, Ohio State University, Columbus, Ohio, United States of America; Center for RNA Biology, Ohio State University, Columbus, Ohio, United States of America.
authors.forename: Venkat
authors.initials: V
authors.lastname: Gopalan
authors.affiliation: Molecular Cellular Developmental Biology Program, Ohio State University, Columbus, Ohio, United States of America; Department of Molecular Genetics, Ohio State University, Columbus, Ohio, United States of America.
authors.forename: Amanda
authors.initials: A
authors.lastname: Simcox
mesh_terms: D000818:Animals; D003445:Crustacea / Q000235:genetics; D004330:Drosophila / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics; D019143:Evolution, Molecular; D005786:Gene Expression Regulation; D023281:Genomics; D007438:Introns / Q000235:genetics; D011401:Promoter Regions, Genetic; D012320:RNA Polymerase III / Q000235:genetics; D016337:RNA, Catalytic / Q000235:genetics*; D012343:RNA, Transfer / Q000235:genetics; D043262:Ribonuclease P / Q000235:genetics*
chemical_list: D016337:RNA, Catalytic; D012343:RNA, Transfer; D012320:RNA Polymerase III; D043262:Ribonuclease P