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Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family

BACKGROUND: Among the 13 families of early-diverging eudicots, only Circaeasteraceae (Ranunculales), which consists of the two monotypic genera Circaeaster and Kingdonia, lacks a published complete plastome sequence. In addition, the phylogenetic position of Circaeasteraceae as sister to Lardizabala...

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Autores principales: Sun, Yanxia, Moore, Michael J., Lin, Nan, Adelalu, Kole F., Meng, Aiping, Jian, Shuguang, Yang, Linsen, Li, Jianqiang, Wang, Hengchang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5551029/
https://www.ncbi.nlm.nih.gov/pubmed/28793854
http://dx.doi.org/10.1186/s12864-017-3956-3
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author Sun, Yanxia
Moore, Michael J.
Lin, Nan
Adelalu, Kole F.
Meng, Aiping
Jian, Shuguang
Yang, Linsen
Li, Jianqiang
Wang, Hengchang
author_facet Sun, Yanxia
Moore, Michael J.
Lin, Nan
Adelalu, Kole F.
Meng, Aiping
Jian, Shuguang
Yang, Linsen
Li, Jianqiang
Wang, Hengchang
author_sort Sun, Yanxia
collection PubMed
description BACKGROUND: Among the 13 families of early-diverging eudicots, only Circaeasteraceae (Ranunculales), which consists of the two monotypic genera Circaeaster and Kingdonia, lacks a published complete plastome sequence. In addition, the phylogenetic position of Circaeasteraceae as sister to Lardizabalaceae has only been weakly or moderately supported in previous studies using smaller data sets. Moreover, previous plastome studies have documented a number of novel structural rearrangements among early-divergent eudicots. Hence it is important to sequence plastomes from Circaeasteraceae to better understand plastome evolution in early-diverging eudicots and to further investigate the phylogenetic position of Circaeasteraceae. RESULTS: Using an Illumina HiSeq 2000, complete plastomes were sequenced from both living members of Circaeasteraceae: Circaeaster agrestis and Kingdonia uniflora. Plastome structure and gene content were compared between these two plastomes, and with those of other early-diverging eudicot plastomes. Phylogenetic analysis of a 79-gene, 99-taxon data set including exemplars of all families of early-diverging eudicots was conducted to resolve the phylogenetic position of Circaeasteraceae. Both plastomes possess the typical quadripartite structure of land plant plastomes. However, a large ~49 kb inversion and a small ~3.5 kb inversion were found in the large single-copy regions of both plastomes, while Circaeaster possesses a number of other rearrangements, particularly in the Inverted Repeat. In addition, infA was found to be a pseudogene and accD was found to be absent within Circaeaster, whereas all ndh genes, except for ndhE and ndhJ, were found to be either pseudogenized (ΨndhA, ΨndhB, ΨndhD, ΨndhH and ΨndhK) or absent (ndhC, ndhF, ndhI and ndhG) in Kingdonia. Circaeasteraceae was strongly supported as sister to Lardizabalaceae in phylogenetic analyses. CONCLUSION: The first plastome sequencing of Circaeasteraceae resulted in the discovery of several unusual rearrangements and the loss of ndh genes, and confirms the sister relationship between Circaeasteraceae and Lardizabalaceae. This research provides new insight to characterize plastome structural evolution in early-diverging eudicots and to better understand relationships within Ranunculales. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3956-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-55510292017-08-14 Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family Sun, Yanxia Moore, Michael J. Lin, Nan Adelalu, Kole F. Meng, Aiping Jian, Shuguang Yang, Linsen Li, Jianqiang Wang, Hengchang BMC Genomics Research Article BACKGROUND: Among the 13 families of early-diverging eudicots, only Circaeasteraceae (Ranunculales), which consists of the two monotypic genera Circaeaster and Kingdonia, lacks a published complete plastome sequence. In addition, the phylogenetic position of Circaeasteraceae as sister to Lardizabalaceae has only been weakly or moderately supported in previous studies using smaller data sets. Moreover, previous plastome studies have documented a number of novel structural rearrangements among early-divergent eudicots. Hence it is important to sequence plastomes from Circaeasteraceae to better understand plastome evolution in early-diverging eudicots and to further investigate the phylogenetic position of Circaeasteraceae. RESULTS: Using an Illumina HiSeq 2000, complete plastomes were sequenced from both living members of Circaeasteraceae: Circaeaster agrestis and Kingdonia uniflora. Plastome structure and gene content were compared between these two plastomes, and with those of other early-diverging eudicot plastomes. Phylogenetic analysis of a 79-gene, 99-taxon data set including exemplars of all families of early-diverging eudicots was conducted to resolve the phylogenetic position of Circaeasteraceae. Both plastomes possess the typical quadripartite structure of land plant plastomes. However, a large ~49 kb inversion and a small ~3.5 kb inversion were found in the large single-copy regions of both plastomes, while Circaeaster possesses a number of other rearrangements, particularly in the Inverted Repeat. In addition, infA was found to be a pseudogene and accD was found to be absent within Circaeaster, whereas all ndh genes, except for ndhE and ndhJ, were found to be either pseudogenized (ΨndhA, ΨndhB, ΨndhD, ΨndhH and ΨndhK) or absent (ndhC, ndhF, ndhI and ndhG) in Kingdonia. Circaeasteraceae was strongly supported as sister to Lardizabalaceae in phylogenetic analyses. CONCLUSION: The first plastome sequencing of Circaeasteraceae resulted in the discovery of several unusual rearrangements and the loss of ndh genes, and confirms the sister relationship between Circaeasteraceae and Lardizabalaceae. This research provides new insight to characterize plastome structural evolution in early-diverging eudicots and to better understand relationships within Ranunculales. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3956-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-09 /pmc/articles/PMC5551029/ /pubmed/28793854 http://dx.doi.org/10.1186/s12864-017-3956-3 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Sun, Yanxia
Moore, Michael J.
Lin, Nan
Adelalu, Kole F.
Meng, Aiping
Jian, Shuguang
Yang, Linsen
Li, Jianqiang
Wang, Hengchang
Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title_full Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title_fullStr Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title_full_unstemmed Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title_short Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
title_sort complete plastome sequencing of both living species of circaeasteraceae (ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5551029/
https://www.ncbi.nlm.nih.gov/pubmed/28793854
http://dx.doi.org/10.1186/s12864-017-3956-3
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