Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals.
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). E...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2015-01-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC4287351?pdf=render |
| _version_ | 1811273249506459648 |
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| author | Sathiya N Manivannan Lien B Lai Venkat Gopalan Amanda Simcox |
| author_facet | Sathiya N Manivannan Lien B Lai Venkat Gopalan Amanda Simcox |
| author_sort | Sathiya N Manivannan |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T22:55:45Z |
| format | Article |
| id | doaj.art-6f749278d895493495c13ff5dd0ef7a6 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-12T22:55:45Z |
| publishDate | 2015-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-6f749278d895493495c13ff5dd0ef7a62022-12-22T03:13:11ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-01-01111e100489310.1371/journal.pgen.1004893Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals.Sathiya N ManivannanLien B LaiVenkat GopalanAmanda SimcoxRibonuclease 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.http://europepmc.org/articles/PMC4287351?pdf=render |
| spellingShingle | Sathiya N Manivannan Lien B Lai Venkat Gopalan Amanda Simcox Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. PLoS Genetics |
| title | Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. |
| title_full | Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. |
| title_fullStr | Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. |
| title_full_unstemmed | Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. |
| title_short | Transcriptional control of an essential ribozyme in Drosophila reveals an ancient evolutionary divide in animals. |
| title_sort | transcriptional control of an essential ribozyme in drosophila reveals an ancient evolutionary divide in animals |
| url | http://europepmc.org/articles/PMC4287351?pdf=render |
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