The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions

Abstract Background Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast g...

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Main Authors: Yan-Yan Guo, Jia-Xing Yang, Ming-Zhu Bai, Guo-Qiang Zhang, Zhong-Jian Liu
Format: Article
Language:English
Published: BMC 2021-05-01
Series:BMC Plant Biology
Subjects:
IR
Online Access:https://doi.org/10.1186/s12870-021-03053-y
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spelling doaj-8a92b35365584db187eaf48c0652b0d42021-06-06T11:19:04ZengBMCBMC Plant Biology1471-22292021-05-0121111410.1186/s12870-021-03053-yThe chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regionsYan-Yan Guo0Jia-Xing Yang1Ming-Zhu Bai2Guo-Qiang Zhang3Zhong-Jian Liu4College of Plant Protection, Henan Agricultural UniversityCollege of Plant Protection, Henan Agricultural UniversityCollege of Plant Protection, Henan Agricultural UniversityKey Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, Shenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Center of China, The Orchid Conservation and Research Center of ShenzhenKey Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization At College of Landscape Architecture, Fujian Agriculture and Forestry UniversityAbstract Background Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Results Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species (size range of 152,130 – 164,092 bp). The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum. The plastomes of Paphiopedilum have a conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of the inverted repeat and small single copy region (IR/SSC) varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates. Conclusions We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.https://doi.org/10.1186/s12870-021-03053-yOrchidaceaePaphiopedilumPhylogenomicsPlastomeBoundary shiftIR
collection DOAJ
language English
format Article
sources DOAJ
author Yan-Yan Guo
Jia-Xing Yang
Ming-Zhu Bai
Guo-Qiang Zhang
Zhong-Jian Liu
spellingShingle Yan-Yan Guo
Jia-Xing Yang
Ming-Zhu Bai
Guo-Qiang Zhang
Zhong-Jian Liu
The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
BMC Plant Biology
Orchidaceae
Paphiopedilum
Phylogenomics
Plastome
Boundary shift
IR
author_facet Yan-Yan Guo
Jia-Xing Yang
Ming-Zhu Bai
Guo-Qiang Zhang
Zhong-Jian Liu
author_sort Yan-Yan Guo
title The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
title_short The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
title_full The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
title_fullStr The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
title_full_unstemmed The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions
title_sort chloroplast genome evolution of venus slipper (paphiopedilum): ir expansion, ssc contraction, and highly rearranged ssc regions
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2021-05-01
description Abstract Background Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Results Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species (size range of 152,130 – 164,092 bp). The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum. The plastomes of Paphiopedilum have a conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of the inverted repeat and small single copy region (IR/SSC) varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates. Conclusions We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.
topic Orchidaceae
Paphiopedilum
Phylogenomics
Plastome
Boundary shift
IR
url https://doi.org/10.1186/s12870-021-03053-y
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