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Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae

BACKGROUND: Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but mo...

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Autores principales: Park, Seongjun, Jansen, Robert K, Park, SeonJoo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4329224/
https://www.ncbi.nlm.nih.gov/pubmed/25652741
http://dx.doi.org/10.1186/s12870-015-0432-6
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author Park, Seongjun
Jansen, Robert K
Park, SeonJoo
author_facet Park, Seongjun
Jansen, Robert K
Park, SeonJoo
author_sort Park, Seongjun
collection PubMed
description BACKGROUND: Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes accD, infA, rpl22, and rpl32. RESULTS: The complete plastid genome of Thalictrum coreanum, the first from the subfamily Thalictroideae (Ranunculaceae), was sequenced and revealed the losses of two genes, infA and rpl32. The functional transfer of these two genes to the nucleus in Thalictrum was verified by examination of nuclear transcriptomes. A survey of the phylogenetic distribution of the rpl32 loss was performed using 17 species of Thalictrum and representatives of related genera in the subfamily Thalictroideae. The plastid-encoded rpl32 gene is likely nonfunctional in members of the subfamily Thalictroideae (Aquilegia, Enemion, Isopyrum, Leptopyrum, Paraquilegia, and Semiaquilegia) including 17 Thalictrum species due to the presence of indels that disrupt the reading frame. A nuclear-encoded rpl32 with high sequence identity was identified in both Thalictrum and Aquilegia. The phylogenetic distribution of this gene loss/transfer and the high level of sequence similarity in transit peptides suggest a single transfer of the plastid-encoded rpl32 to the nucleus in the ancestor of the subfamily Thalictroideae approximately 20–32 Mya. CONCLUSIONS: The genome sequence of Thalictrum coreanum provides valuable information for improving the understanding of the evolution of plastid genomes within Ranunculaceae and across angiosperms. Thalictrum is unusual among the three sequenced Ranunculaceae plastid genomes in the loss of two genes infA and rpl32, which have been functionally transferred to the nucleus. In the case of rpl32 this represents the third documented independent transfer from the plastid to the nucleus with the other two transfers occurring in the unrelated angiosperm families Rhizophoraceae and Salicaceae. Furthermore, the transfer of rpl32 provides additional molecular evidence for the monophyly of the subfamily Thalictroideae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0432-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-43292242015-02-16 Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae Park, Seongjun Jansen, Robert K Park, SeonJoo BMC Plant Biol Research Article BACKGROUND: Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes accD, infA, rpl22, and rpl32. RESULTS: The complete plastid genome of Thalictrum coreanum, the first from the subfamily Thalictroideae (Ranunculaceae), was sequenced and revealed the losses of two genes, infA and rpl32. The functional transfer of these two genes to the nucleus in Thalictrum was verified by examination of nuclear transcriptomes. A survey of the phylogenetic distribution of the rpl32 loss was performed using 17 species of Thalictrum and representatives of related genera in the subfamily Thalictroideae. The plastid-encoded rpl32 gene is likely nonfunctional in members of the subfamily Thalictroideae (Aquilegia, Enemion, Isopyrum, Leptopyrum, Paraquilegia, and Semiaquilegia) including 17 Thalictrum species due to the presence of indels that disrupt the reading frame. A nuclear-encoded rpl32 with high sequence identity was identified in both Thalictrum and Aquilegia. The phylogenetic distribution of this gene loss/transfer and the high level of sequence similarity in transit peptides suggest a single transfer of the plastid-encoded rpl32 to the nucleus in the ancestor of the subfamily Thalictroideae approximately 20–32 Mya. CONCLUSIONS: The genome sequence of Thalictrum coreanum provides valuable information for improving the understanding of the evolution of plastid genomes within Ranunculaceae and across angiosperms. Thalictrum is unusual among the three sequenced Ranunculaceae plastid genomes in the loss of two genes infA and rpl32, which have been functionally transferred to the nucleus. In the case of rpl32 this represents the third documented independent transfer from the plastid to the nucleus with the other two transfers occurring in the unrelated angiosperm families Rhizophoraceae and Salicaceae. Furthermore, the transfer of rpl32 provides additional molecular evidence for the monophyly of the subfamily Thalictroideae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0432-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-02-05 /pmc/articles/PMC4329224/ /pubmed/25652741 http://dx.doi.org/10.1186/s12870-015-0432-6 Text en © Park et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Park, Seongjun
Jansen, Robert K
Park, SeonJoo
Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title_full Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title_fullStr Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title_full_unstemmed Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title_short Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae
title_sort complete plastome sequence of thalictrum coreanum (ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily thalictroideae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4329224/
https://www.ncbi.nlm.nih.gov/pubmed/25652741
http://dx.doi.org/10.1186/s12870-015-0432-6
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