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). Eukary...

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Main Authors:	Manivannan, Sathiya N., Lai, Lien B., Gopalan, Venkat, Simcox, Amanda
Format:	Online
Language:	English
Published:	Public Library of Science 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4287351/

id	pubmed-4287351
recordtype	oai_dc
spelling	pubmed-42873512015-01-12 Transcriptional Control of an Essential Ribozyme in Drosophila Reveals an Ancient Evolutionary Divide in Animals Manivannan, Sathiya N. Lai, Lien B. Gopalan, Venkat Simcox, Amanda Research Article 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. Public Library of Science 2015-01-08 /pmc/articles/PMC4287351/ /pubmed/25569672 http://dx.doi.org/10.1371/journal.pgen.1004893 Text en © 2015 Manivannan et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Manivannan, Sathiya N. Lai, Lien B. Gopalan, Venkat Simcox, Amanda
spellingShingle	Manivannan, Sathiya N. Lai, Lien B. Gopalan, Venkat Simcox, Amanda Transcriptional Control of an Essential Ribozyme in Drosophila Reveals an Ancient Evolutionary Divide in Animals
author_facet	Manivannan, Sathiya N. Lai, Lien B. Gopalan, Venkat Simcox, Amanda
author_sort	Manivannan, Sathiya N.
title	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_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_sort	transcriptional control of an essential ribozyme in drosophila reveals an ancient evolutionary divide in animals
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.
publisher	Public Library of Science
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4287351/
_version_	1613174284032671744

Transcriptional Control of an Essential Ribozyme in Drosophila Reveals an Ancient Evolutionary Divide in Animals

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