Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance
Most DNA in the genomes of higher organisms does not code for proteins. RNA Polymerase II (Pol II) transcribes non-coding DNA into long non-coding RNAs (lncRNAs), but biological roles of lncRNA are unclear. We find that mutations in the yeast lncRNA CUT60 result in poor growth. Defective termination...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-03-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/31989 |
| _version_ | 1811200038334889984 |
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| author | Dorine Jeanne Mariëtte du Mee Maxim Ivanov Joseph Paul Parker Stephen Buratowski Sebastian Marquardt |
| author_facet | Dorine Jeanne Mariëtte du Mee Maxim Ivanov Joseph Paul Parker Stephen Buratowski Sebastian Marquardt |
| author_sort | Dorine Jeanne Mariëtte du Mee |
| collection | DOAJ |
| description | Most DNA in the genomes of higher organisms does not code for proteins. RNA Polymerase II (Pol II) transcribes non-coding DNA into long non-coding RNAs (lncRNAs), but biological roles of lncRNA are unclear. We find that mutations in the yeast lncRNA CUT60 result in poor growth. Defective termination of CUT60 transcription causes read-through transcription across the ATP16 gene promoter. Read-through transcription localizes chromatin signatures associated with Pol II elongation to the ATP16 promoter. The act of Pol II elongation across this promoter represses functional ATP16 expression by a Transcriptional Interference (TI) mechanism. Atp16p function in the mitochondrial ATP-synthase complex promotes mitochondrial DNA stability. ATP16 repression by TI through inefficient termination of CUT60 therefore triggers mitochondrial genome loss. Our results expand the functional and mechanistic implications of non-coding DNA in eukaryotes by highlighting termination of nuclear lncRNA transcription as mechanism to stabilize an organellar genome. |
| first_indexed | 2024-04-12T01:58:01Z |
| format | Article |
| id | doaj.art-6d63143c8c6041d286974897936fc05c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T01:58:01Z |
| publishDate | 2018-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-6d63143c8c6041d286974897936fc05c2022-12-22T03:52:45ZengeLife Sciences Publications LtdeLife2050-084X2018-03-01710.7554/eLife.31989Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenanceDorine Jeanne Mariëtte du Mee0https://orcid.org/0000-0002-0037-7882Maxim Ivanov1https://orcid.org/0000-0001-7548-3316Joseph Paul Parker2Stephen Buratowski3https://orcid.org/0000-0003-0440-3926Sebastian Marquardt4https://orcid.org/0000-0003-1709-2717Department of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, DenmarkDepartment of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, DenmarkDepartment of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, DenmarkDepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, United StatesDepartment of Plant and Environmental Sciences, Copenhagen Plant Science Centre, University of Copenhagen, Frederiksberg, DenmarkMost DNA in the genomes of higher organisms does not code for proteins. RNA Polymerase II (Pol II) transcribes non-coding DNA into long non-coding RNAs (lncRNAs), but biological roles of lncRNA are unclear. We find that mutations in the yeast lncRNA CUT60 result in poor growth. Defective termination of CUT60 transcription causes read-through transcription across the ATP16 gene promoter. Read-through transcription localizes chromatin signatures associated with Pol II elongation to the ATP16 promoter. The act of Pol II elongation across this promoter represses functional ATP16 expression by a Transcriptional Interference (TI) mechanism. Atp16p function in the mitochondrial ATP-synthase complex promotes mitochondrial DNA stability. ATP16 repression by TI through inefficient termination of CUT60 therefore triggers mitochondrial genome loss. Our results expand the functional and mechanistic implications of non-coding DNA in eukaryotes by highlighting termination of nuclear lncRNA transcription as mechanism to stabilize an organellar genome.https://elifesciences.org/articles/31989RNA Polymerase IIlncRNATranscriptional InterferenceChromatinPervasive transcriptionGenome Stability |
| spellingShingle | Dorine Jeanne Mariëtte du Mee Maxim Ivanov Joseph Paul Parker Stephen Buratowski Sebastian Marquardt Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance eLife RNA Polymerase II lncRNA Transcriptional Interference Chromatin Pervasive transcription Genome Stability |
| title | Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance |
| title_full | Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance |
| title_fullStr | Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance |
| title_full_unstemmed | Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance |
| title_short | Efficient termination of nuclear lncRNA transcription promotes mitochondrial genome maintenance |
| title_sort | efficient termination of nuclear lncrna transcription promotes mitochondrial genome maintenance |
| topic | RNA Polymerase II lncRNA Transcriptional Interference Chromatin Pervasive transcription Genome Stability |
| url | https://elifesciences.org/articles/31989 |
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