Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region

With c. 2,000 species, Euphorbia is one of the largest angiosperm genera, yet a lack of chloroplast genome (plastome) resources impedes a better understanding of its evolution. In this study, we assembled and annotated 28 plastomes from Euphorbiaceae, of which 15 were newly sequenced. Phylogenomic a...

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Main Authors: Neng Wei, Oscar A. Pérez-Escobar, Paul M. Musili, Wei-Chang Huang, Jun-Bo Yang, Ai-Qun Hu, Guang-Wan Hu, Olwen M. Grace, Qing-Feng Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.712064/full
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author Neng Wei
Neng Wei
Neng Wei
Neng Wei
Oscar A. Pérez-Escobar
Paul M. Musili
Wei-Chang Huang
Jun-Bo Yang
Ai-Qun Hu
Guang-Wan Hu
Guang-Wan Hu
Guang-Wan Hu
Olwen M. Grace
Qing-Feng Wang
Qing-Feng Wang
Qing-Feng Wang
author_facet Neng Wei
Neng Wei
Neng Wei
Neng Wei
Oscar A. Pérez-Escobar
Paul M. Musili
Wei-Chang Huang
Jun-Bo Yang
Ai-Qun Hu
Guang-Wan Hu
Guang-Wan Hu
Guang-Wan Hu
Olwen M. Grace
Qing-Feng Wang
Qing-Feng Wang
Qing-Feng Wang
author_sort Neng Wei
collection DOAJ
description With c. 2,000 species, Euphorbia is one of the largest angiosperm genera, yet a lack of chloroplast genome (plastome) resources impedes a better understanding of its evolution. In this study, we assembled and annotated 28 plastomes from Euphorbiaceae, of which 15 were newly sequenced. Phylogenomic and comparative analyses of 22 plastome sequences from all four recognized subgenera within Euphorbia revealed that plastome length in Euphorbia is labile, presenting a range of variation c. 42 kb. Large-scale expansions of the inverted repeat (IR) region were identified, and at the extreme opposite, the near-complete loss of the IR region (with only 355 bp left) was detected for the first time in Euphorbiaceae. Other structural variations, including gene inversion and duplication, and gene loss/pseudogenization, were also observed. We screened the most promising molecular markers from both intergenic and coding regions for phylogeny-based utilities, and estimated maximum likelihood and Bayesian phylogenies from four datasets including whole plastome sequences. The monophyly of Euphorbia is supported, and its four subgenera are recovered in a successive sister relationship. Our study constitutes the first comprehensive investigation on the plastome structural variation in Euphorbia and it provides resources for phylogenetic research in the genus, facilitating further studies on its taxonomy, evolution, and conservation.
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spelling doaj.art-9179dce237a74e5a935652133b3133122022-12-21T22:12:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-08-011210.3389/fpls.2021.712064712064Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat RegionNeng Wei0Neng Wei1Neng Wei2Neng Wei3Oscar A. Pérez-Escobar4Paul M. Musili5Wei-Chang Huang6Jun-Bo Yang7Ai-Qun Hu8Guang-Wan Hu9Guang-Wan Hu10Guang-Wan Hu11Olwen M. Grace12Qing-Feng Wang13Qing-Feng Wang14Qing-Feng Wang15Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaRoyal Botanic Gardens, Kew, Richmond, United KingdomCenter of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaRoyal Botanic Gardens, Kew, Richmond, United KingdomEast African Herbarium, National Museums of Kenya, Nairobi, KenyaShanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Chenshan Botanical Garden, Shanghai, ChinaGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, ChinaRoyal Botanic Gardens, Kew, Richmond, United KingdomKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCenter of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan, ChinaSino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, ChinaRoyal Botanic Gardens, Kew, Richmond, United KingdomKey Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCenter of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan, ChinaSino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, ChinaWith c. 2,000 species, Euphorbia is one of the largest angiosperm genera, yet a lack of chloroplast genome (plastome) resources impedes a better understanding of its evolution. In this study, we assembled and annotated 28 plastomes from Euphorbiaceae, of which 15 were newly sequenced. Phylogenomic and comparative analyses of 22 plastome sequences from all four recognized subgenera within Euphorbia revealed that plastome length in Euphorbia is labile, presenting a range of variation c. 42 kb. Large-scale expansions of the inverted repeat (IR) region were identified, and at the extreme opposite, the near-complete loss of the IR region (with only 355 bp left) was detected for the first time in Euphorbiaceae. Other structural variations, including gene inversion and duplication, and gene loss/pseudogenization, were also observed. We screened the most promising molecular markers from both intergenic and coding regions for phylogeny-based utilities, and estimated maximum likelihood and Bayesian phylogenies from four datasets including whole plastome sequences. The monophyly of Euphorbia is supported, and its four subgenera are recovered in a successive sister relationship. Our study constitutes the first comprehensive investigation on the plastome structural variation in Euphorbia and it provides resources for phylogenetic research in the genus, facilitating further studies on its taxonomy, evolution, and conservation.https://www.frontiersin.org/articles/10.3389/fpls.2021.712064/fullcomparative genomicsorganellar evolutionphylogenetic inferenceplastome rearrangementspurge familystructural variations
spellingShingle Neng Wei
Neng Wei
Neng Wei
Neng Wei
Oscar A. Pérez-Escobar
Paul M. Musili
Wei-Chang Huang
Jun-Bo Yang
Ai-Qun Hu
Guang-Wan Hu
Guang-Wan Hu
Guang-Wan Hu
Olwen M. Grace
Qing-Feng Wang
Qing-Feng Wang
Qing-Feng Wang
Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
Frontiers in Plant Science
comparative genomics
organellar evolution
phylogenetic inference
plastome rearrangement
spurge family
structural variations
title Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
title_full Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
title_fullStr Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
title_full_unstemmed Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
title_short Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region
title_sort plastome evolution in the hyperdiverse genus euphorbia euphorbiaceae using phylogenomic and comparative analyses large scale expansion and contraction of the inverted repeat region
topic comparative genomics
organellar evolution
phylogenetic inference
plastome rearrangement
spurge family
structural variations
url https://www.frontiersin.org/articles/10.3389/fpls.2021.712064/full
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