Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists

Organelle genomes are among the most sequenced kinds of chromosome. This is largely because they are small and widely used in molecular studies, but also because next-generation sequencing technologies made sequencing easier, faster, and cheaper. However, studies of organelle RNA have not kept pace...

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Main Authors: Matheus Sanitá Lima, David Roy Smith
Format: Article
Language:English
Published: Oxford University Press 2017-11-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.117.300290
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spelling doaj-4333f49056ac4367b631ce3e085122cf2021-07-02T07:06:28ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362017-11-017113789379610.1534/g3.117.30029020Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing ProtistsMatheus Sanitá LimaDavid Roy SmithOrganelle genomes are among the most sequenced kinds of chromosome. This is largely because they are small and widely used in molecular studies, but also because next-generation sequencing technologies made sequencing easier, faster, and cheaper. However, studies of organelle RNA have not kept pace with those of DNA, despite huge amounts of freely available eukaryotic RNA-sequencing (RNA-seq) data. Little is known about organelle transcription in nonmodel species, and most of the available eukaryotic RNA-seq data have not been mined for organelle transcripts. Here, we use publicly available RNA-seq experiments to investigate organelle transcription in 30 diverse plastid-bearing protists with varying organelle genomic architectures. Mapping RNA-seq data to organelle genomes revealed pervasive, genome-wide transcription, regardless of the taxonomic grouping, gene organization, or noncoding content. For every species analyzed, transcripts covered ≥85% of the mitochondrial and/or plastid genomes (all of which were ≤105 kb), indicating that most of the organelle DNA—coding and noncoding—is transcriptionally active. These results follow earlier studies of model species showing that organellar transcription is coupled and ubiquitous across the genome, requiring significant downstream processing of polycistronic transcripts. Our findings suggest that noncoding organelle DNA can be transcriptionally active, raising questions about the underlying function of these transcripts and underscoring the utility of publicly available RNA-seq data for recovering complete genome sequences. If pervasive transcription is also found in bigger organelle genomes (>105 kb) and across a broader range of eukaryotes, this could indicate that noncoding organelle RNAs are regulating fundamental processes within eukaryotic cells.http://g3journal.org/lookup/doi/10.1534/g3.117.300290RNA-seqmitochondrial transcriptionorganelle gene expressionplastid transcriptionprotists
collection DOAJ
language English
format Article
sources DOAJ
author Matheus Sanitá Lima
David Roy Smith
spellingShingle Matheus Sanitá Lima
David Roy Smith
Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
G3: Genes, Genomes, Genetics
RNA-seq
mitochondrial transcription
organelle gene expression
plastid transcription
protists
author_facet Matheus Sanitá Lima
David Roy Smith
author_sort Matheus Sanitá Lima
title Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
title_short Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
title_full Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
title_fullStr Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
title_full_unstemmed Pervasive, Genome-Wide Transcription in the Organelle Genomes of Diverse Plastid-Bearing Protists
title_sort pervasive, genome-wide transcription in the organelle genomes of diverse plastid-bearing protists
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2017-11-01
description Organelle genomes are among the most sequenced kinds of chromosome. This is largely because they are small and widely used in molecular studies, but also because next-generation sequencing technologies made sequencing easier, faster, and cheaper. However, studies of organelle RNA have not kept pace with those of DNA, despite huge amounts of freely available eukaryotic RNA-sequencing (RNA-seq) data. Little is known about organelle transcription in nonmodel species, and most of the available eukaryotic RNA-seq data have not been mined for organelle transcripts. Here, we use publicly available RNA-seq experiments to investigate organelle transcription in 30 diverse plastid-bearing protists with varying organelle genomic architectures. Mapping RNA-seq data to organelle genomes revealed pervasive, genome-wide transcription, regardless of the taxonomic grouping, gene organization, or noncoding content. For every species analyzed, transcripts covered ≥85% of the mitochondrial and/or plastid genomes (all of which were ≤105 kb), indicating that most of the organelle DNA—coding and noncoding—is transcriptionally active. These results follow earlier studies of model species showing that organellar transcription is coupled and ubiquitous across the genome, requiring significant downstream processing of polycistronic transcripts. Our findings suggest that noncoding organelle DNA can be transcriptionally active, raising questions about the underlying function of these transcripts and underscoring the utility of publicly available RNA-seq data for recovering complete genome sequences. If pervasive transcription is also found in bigger organelle genomes (>105 kb) and across a broader range of eukaryotes, this could indicate that noncoding organelle RNAs are regulating fundamental processes within eukaryotic cells.
topic RNA-seq
mitochondrial transcription
organelle gene expression
plastid transcription
protists
url http://g3journal.org/lookup/doi/10.1534/g3.117.300290
work_keys_str_mv AT matheussanitalima pervasivegenomewidetranscriptionintheorganellegenomesofdiverseplastidbearingprotists
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