Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)

Abstract Background The columbine genus (Aquilegia) contains many species with horticultural and pharmaceutical importance. However, a well-resolved phylogeny for this genus remains lacking owing to recent and rapid radiation. We obtained plastomes of 75 Aquilegia species and six species of other ge...

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Main Authors: Fang-Min Yu, Wen-Chuang He, Andrey S. Erst, Huan-Wen Peng, Yuan-Yuan Ling, Tatyana V. Erst, Michael V. Bardukov, Wei Wang, Kun-Li Xiang
Format: Article
Language:English
Published: BMC 2025-08-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-07093-6
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author Fang-Min Yu
Wen-Chuang He
Andrey S. Erst
Huan-Wen Peng
Yuan-Yuan Ling
Tatyana V. Erst
Michael V. Bardukov
Wei Wang
Kun-Li Xiang
author_facet Fang-Min Yu
Wen-Chuang He
Andrey S. Erst
Huan-Wen Peng
Yuan-Yuan Ling
Tatyana V. Erst
Michael V. Bardukov
Wei Wang
Kun-Li Xiang
author_sort Fang-Min Yu
collection DOAJ
description Abstract Background The columbine genus (Aquilegia) contains many species with horticultural and pharmaceutical importance. However, a well-resolved phylogeny for this genus remains lacking owing to recent and rapid radiation. We obtained plastomes of 75 Aquilegia species and six species of other genera in Thalictroideae to reconstruct a robust phylogeny for Aquilegia. Within the phylogenetic framework, we investigated the evolutionary patterns of structural variations in Aquilegia plastomes. We also examined appropriate molecular markers for species identification of this genus. Results Plastid phylogenomic analyses show that Aquilegia is monophyletic and divided into two major clades and eight subclades, largely in agreement with species geographical distributions. Aquilegia plastomes have copy number variations (CNVs) of genes at the boundaries of IR/SC regions. An inversion was identified in the large single-copy region (LSC) plastomes of Aquilegia, Semiaquilegia, and Urophysa. The inversion was adjacent to three distinct structures (type I-III) in LSC region, each characterized by presence or absence of different short inverted repeat (sIR) regions. The most recent common ancestor of Aquilegia species was type III, and other two types were derived by shortening or loss of sIRs. Ten hypervariable regions were identified in Aquilegia plastomes. Conclusions We present a well-resolved phylogeny for Aquilegia. The CNVs of genes were observed frequently at the boundaries of IR/SC regions and sIR regions in the genus, and the inversions and sIR in LSC regions have phylogenetic signal and lead to notable variations in gene content and length of plastomes. The new hypervariable regions can be used for phylogenetic analyses and molecular identification of Aquilegia. This study provides new insights into the structural evolution of plastome in angiosperms, and also have important implications for the conservation and utilization of Aquilegia species.
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spelling doaj-art-e5c6b73320274383a4a91b0e3ed8cec32025-08-24T11:16:47ZengBMCBMC Plant Biology1471-22292025-08-0125111310.1186/s12870-025-07093-6Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)Fang-Min Yu0Wen-Chuang He1Andrey S. Erst2Huan-Wen Peng3Yuan-Yuan Ling4Tatyana V. Erst5Michael V. Bardukov6Wei Wang7Kun-Li Xiang8State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesCentral Siberian Botanical Garden, Siberian Branch of Russian Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesInstitute of Cytology and Genetics, Siberian Branch of Russian Academy of SciencesCentral Siberian Botanical Garden, Siberian Branch of Russian Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of SciencesAbstract Background The columbine genus (Aquilegia) contains many species with horticultural and pharmaceutical importance. However, a well-resolved phylogeny for this genus remains lacking owing to recent and rapid radiation. We obtained plastomes of 75 Aquilegia species and six species of other genera in Thalictroideae to reconstruct a robust phylogeny for Aquilegia. Within the phylogenetic framework, we investigated the evolutionary patterns of structural variations in Aquilegia plastomes. We also examined appropriate molecular markers for species identification of this genus. Results Plastid phylogenomic analyses show that Aquilegia is monophyletic and divided into two major clades and eight subclades, largely in agreement with species geographical distributions. Aquilegia plastomes have copy number variations (CNVs) of genes at the boundaries of IR/SC regions. An inversion was identified in the large single-copy region (LSC) plastomes of Aquilegia, Semiaquilegia, and Urophysa. The inversion was adjacent to three distinct structures (type I-III) in LSC region, each characterized by presence or absence of different short inverted repeat (sIR) regions. The most recent common ancestor of Aquilegia species was type III, and other two types were derived by shortening or loss of sIRs. Ten hypervariable regions were identified in Aquilegia plastomes. Conclusions We present a well-resolved phylogeny for Aquilegia. The CNVs of genes were observed frequently at the boundaries of IR/SC regions and sIR regions in the genus, and the inversions and sIR in LSC regions have phylogenetic signal and lead to notable variations in gene content and length of plastomes. The new hypervariable regions can be used for phylogenetic analyses and molecular identification of Aquilegia. This study provides new insights into the structural evolution of plastome in angiosperms, and also have important implications for the conservation and utilization of Aquilegia species.https://doi.org/10.1186/s12870-025-07093-6AquilegiaPlastid genomeStructures variationPhylogenyHypervariable region
spellingShingle Fang-Min Yu
Wen-Chuang He
Andrey S. Erst
Huan-Wen Peng
Yuan-Yuan Ling
Tatyana V. Erst
Michael V. Bardukov
Wei Wang
Kun-Li Xiang
Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
BMC Plant Biology
Aquilegia
Plastid genome
Structures variation
Phylogeny
Hypervariable region
title Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
title_full Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
title_fullStr Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
title_full_unstemmed Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
title_short Phylogenomics and structural variations of plastid genomes of the columbine genus (Ranunculaceae)
title_sort phylogenomics and structural variations of plastid genomes of the columbine genus ranunculaceae
topic Aquilegia
Plastid genome
Structures variation
Phylogeny
Hypervariable region
url https://doi.org/10.1186/s12870-025-07093-6
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