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

Abstract 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 Lar...

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Main Authors: Yanxia Sun, Michael J. Moore, Nan Lin, Kole F. Adelalu, Aiping Meng, Shuguang Jian, Linsen Yang, Jianqiang Li, Hengchang Wang
Format: Article
Language:English
Published: BMC 2017-08-01
Series:BMC Genomics
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Online Access:http://link.springer.com/article/10.1186/s12864-017-3956-3
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spelling doaj-5e56c6973de54066a0e1b4fc5839b3db2020-11-25T00:43:13ZengBMCBMC Genomics1471-21642017-08-0118111010.1186/s12864-017-3956-3Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene familyYanxia Sun0Michael J. Moore1Nan Lin2Kole F. Adelalu3Aiping Meng4Shuguang Jian5Linsen Yang6Jianqiang Li7Hengchang Wang8Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesDepartment of Biology, Oberlin CollegeKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesSouth China Botanical Garden, Chinese Academy of SciencesHubei Key Laboratory of Shennongjia Golden Monkey Conservation Biology, Administration of Shennongjia National ParkKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of SciencesAbstract 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 .http://link.springer.com/article/10.1186/s12864-017-3956-3Early-diverging eudicotsCircaeasteraceaePlastomeRearrangementsGene lossPhylogenetic analyses
collection DOAJ
language English
format Article
sources DOAJ
author Yanxia Sun
Michael J. Moore
Nan Lin
Kole F. Adelalu
Aiping Meng
Shuguang Jian
Linsen Yang
Jianqiang Li
Hengchang Wang
spellingShingle Yanxia Sun
Michael J. Moore
Nan Lin
Kole F. Adelalu
Aiping Meng
Shuguang Jian
Linsen Yang
Jianqiang Li
Hengchang Wang
Complete plastome sequencing of both living species of Circaeasteraceae (Ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
BMC Genomics
Early-diverging eudicots
Circaeasteraceae
Plastome
Rearrangements
Gene loss
Phylogenetic analyses
author_facet Yanxia Sun
Michael J. Moore
Nan Lin
Kole F. Adelalu
Aiping Meng
Shuguang Jian
Linsen Yang
Jianqiang Li
Hengchang Wang
author_sort Yanxia Sun
title 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_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_sort complete plastome sequencing of both living species of circaeasteraceae (ranunculales) reveals unusual rearrangements and the loss of the ndh gene family
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2017-08-01
description Abstract 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 .
topic Early-diverging eudicots
Circaeasteraceae
Plastome
Rearrangements
Gene loss
Phylogenetic analyses
url http://link.springer.com/article/10.1186/s12864-017-3956-3
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