Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code

The tiny green algae belonging to the Chloropicophyceae play a key role in marine phytoplankton communities; this newly erected class of prasinophytes comprises two genera (Chloropicon and Chloroparvula) containing each several species. We sequenced the plastomes and mitogenomes of eight Chloropicon...

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Main Authors: Turmel, Monique, Lopes dos Santos, Adriana, Otis, Christian, Sergerie, Roxanne, Lemieux, Claude
Other Authors: Archibald, John
Format: Article
Language:English
Published: 2019
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Online Access:https://hdl.handle.net/10356/105927
http://hdl.handle.net/10220/48811
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Institution: Nanyang Technological University
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spelling sg-ntu-dr.10356-1059272023-02-28T16:41:41Z Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code Turmel, Monique Lopes dos Santos, Adriana Otis, Christian Sergerie, Roxanne Lemieux, Claude Archibald, John Asian School of the Environment Prasinophyte Green Algae DRNTU::Engineering::Environmental engineering Picocystis Salinarum The tiny green algae belonging to the Chloropicophyceae play a key role in marine phytoplankton communities; this newly erected class of prasinophytes comprises two genera (Chloropicon and Chloroparvula) containing each several species. We sequenced the plastomes and mitogenomes of eight Chloropicon and five Chloroparvula species to better delineate the phylogenetic affinities of these taxa and to infer the suite of changes that their organelle genomes sustained during evolution. The relationships resolved in organelle-based phylogenomic trees were essentially congruent with previously reported rRNA trees, and similar evolutionary trends but distinct dynamics were identified for the plastome and mitogenome. Although the plastome sustained considerable changes in gene content and order at the time the two genera split, subsequently it remained stable and maintained a very small size. The mitogenome, however, was remodeled more gradually and showed more fluctuation in size, mainly as a result of expansions/contractions of intergenic regions. Remarkably, the plastome and mitogenome lost a common set of three tRNA genes, with the trnI(cau) and trnL(uaa) losses being accompanied with important variations in codon usage. Unexpectedly, despite the disappearance of trnI(cau) from the plastome in the Chloroparvula lineage, AUA codons (the codons recognized by this gene product) were detected in certain plastid genes. By comparing the sequences of plastid protein-coding genes from chloropicophycean and phylogenetically diverse chlorophyte algae with those of the corresponding predicted proteins, we discovered that the AUA codon was reassigned from isoleucine to methionine in Chloroparvula. This noncanonical genetic code has not previously been uncovered in plastids. Published version 2019-06-19T01:40:32Z 2019-12-06T22:00:51Z 2019-06-19T01:40:32Z 2019-12-06T22:00:51Z 2019 Journal Article Turmel, M., Lopes dos Santos, A., Otis, C., Sergerie, R., & Lemieux, C. (2019). Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code. Genome Biology and Evolution, 11(4), 1275-1292. doi: 10.1093/gbe/evz074 https://hdl.handle.net/10356/105927 http://hdl.handle.net/10220/48811 10.1093/gbe/evz074 en Genome Biology and Evolution © 2019 The Author(s). Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com 18 p. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Prasinophyte Green Algae
DRNTU::Engineering::Environmental engineering
Picocystis Salinarum
spellingShingle Prasinophyte Green Algae
DRNTU::Engineering::Environmental engineering
Picocystis Salinarum
Turmel, Monique
Lopes dos Santos, Adriana
Otis, Christian
Sergerie, Roxanne
Lemieux, Claude
Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
description The tiny green algae belonging to the Chloropicophyceae play a key role in marine phytoplankton communities; this newly erected class of prasinophytes comprises two genera (Chloropicon and Chloroparvula) containing each several species. We sequenced the plastomes and mitogenomes of eight Chloropicon and five Chloroparvula species to better delineate the phylogenetic affinities of these taxa and to infer the suite of changes that their organelle genomes sustained during evolution. The relationships resolved in organelle-based phylogenomic trees were essentially congruent with previously reported rRNA trees, and similar evolutionary trends but distinct dynamics were identified for the plastome and mitogenome. Although the plastome sustained considerable changes in gene content and order at the time the two genera split, subsequently it remained stable and maintained a very small size. The mitogenome, however, was remodeled more gradually and showed more fluctuation in size, mainly as a result of expansions/contractions of intergenic regions. Remarkably, the plastome and mitogenome lost a common set of three tRNA genes, with the trnI(cau) and trnL(uaa) losses being accompanied with important variations in codon usage. Unexpectedly, despite the disappearance of trnI(cau) from the plastome in the Chloroparvula lineage, AUA codons (the codons recognized by this gene product) were detected in certain plastid genes. By comparing the sequences of plastid protein-coding genes from chloropicophycean and phylogenetically diverse chlorophyte algae with those of the corresponding predicted proteins, we discovered that the AUA codon was reassigned from isoleucine to methionine in Chloroparvula. This noncanonical genetic code has not previously been uncovered in plastids.
author2 Archibald, John
author_facet Archibald, John
Turmel, Monique
Lopes dos Santos, Adriana
Otis, Christian
Sergerie, Roxanne
Lemieux, Claude
format Article
author Turmel, Monique
Lopes dos Santos, Adriana
Otis, Christian
Sergerie, Roxanne
Lemieux, Claude
author_sort Turmel, Monique
title Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
title_short Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
title_full Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
title_fullStr Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
title_full_unstemmed Tracing the evolution of the plastome and mitogenome in the Chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code
title_sort tracing the evolution of the plastome and mitogenome in the chloropicophyceae uncovered convergent trna gene losses and a variant plastid genetic code
publishDate 2019
url https://hdl.handle.net/10356/105927
http://hdl.handle.net/10220/48811
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