Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses

Abstract Background The genus Sanicula L. is a unique perennial herb that holds important medicinal values. Although the previous studies on Sanicula provided us with a good research basis, its taxonomic system and interspecific relationships have not been satisfactorily resolved, especially for tho...

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Main Authors: Bo-Ni Song, Chang-Kun Liu, An-Qi Zhao, Rong-Ming Tian, Deng-Feng Xie, Yu-Lin Xiao, Huai Chen, Song-Dong Zhou, Xing-Jin He
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-024-04750-0
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author Bo-Ni Song
Chang-Kun Liu
An-Qi Zhao
Rong-Ming Tian
Deng-Feng Xie
Yu-Lin Xiao
Huai Chen
Song-Dong Zhou
Xing-Jin He
author_facet Bo-Ni Song
Chang-Kun Liu
An-Qi Zhao
Rong-Ming Tian
Deng-Feng Xie
Yu-Lin Xiao
Huai Chen
Song-Dong Zhou
Xing-Jin He
author_sort Bo-Ni Song
collection DOAJ
description Abstract Background The genus Sanicula L. is a unique perennial herb that holds important medicinal values. Although the previous studies on Sanicula provided us with a good research basis, its taxonomic system and interspecific relationships have not been satisfactorily resolved, especially for those endemic to China. Moreover, the evolutionary history of this genus also remains inadequately understood. The plastid genomes possessing highly conserved structure and limited evolutionary rate have proved to be an effective tool for studying plant phylogeny and evolution. Results In the current study, we newly sequenced and assembled fifteen Sanicula complete plastomes. Combined with two previously reported plastomes, we performed comprehensively plastid phylogenomics analyses to gain novel insights into the evolutionary history of this genus. The comparative results indicated that the seventeen plastomes exhibited a high degree of conservation and similarity in terms of their structure, size, GC content, gene order, IR borders, codon bias patterns and SSRs profiles. Such as all of them displayed a typical quadripartite structure, including a large single copy region (LSC: 85,074–86,197 bp), a small single copy region (SSC: 17,047–17,132 bp) separated by a pair of inverted repeat regions (IRs: 26,176–26,334 bp). And the seventeen plastomes had similar IR boundaries and the adjacent genes were identical. The rps19 gene was located at the junction of the LSC/IRa, the IRa/SSC junction region was located between the trnN gene and ndhF gene, the ycf1 gene appeared in the SSC/IRb junction and the IRb/LSC boundary was located between rpl12 gene and trnH gene. Twelve specific mutation hotspots (atpF, cemA, accD, rpl22, rbcL, matK, ycf1, trnH-psbA, ycf4-cemA, rbcL-accD, trnE-trnT and trnG-trnR) were identified that can serve as potential DNA barcodes for species identification within the genus Sanicula. Furthermore, the plastomes data and Internal Transcribed Spacer (ITS) sequences were performed to reconstruct the phylogeny of Sanicula. Although the tree topologies of them were incongruent, both provided strong evidence supporting the monophyly of Saniculoideae and Apioideae. In addition, the sister groups between Saniculoideae and Apioideae were strongly suggested. The Sanicula species involved in this study were clustered into a clade, and the Eryngium species were also clustered together. However, it was clearly observed that the sections of Sanicula involved in the current study were not respectively recovered as monophyletic group. Molecular dating analysis explored that the origin of this genus was occurred during the late Eocene period, approximately 37.84 Ma (95% HPD: 20.33–52.21 Ma) years ago and the diversification of the genus was occurred in early Miocene 18.38 Ma (95% HPD: 10.68–25.28 Ma). Conclusion The plastome-based tree and ITS-based tree generated incongruences, which may be attributed to the event of hybridization/introgression, incomplete lineage sorting (ILS) and chloroplast capture. Our study highlighted the power of plastome data to significantly improve the phylogenetic supports and resolutions, and to efficiently explore the evolutionary history of this genus. Molecular dating analysis explored that the diversification of the genus occurred in the early Miocene, which was largely influenced by the prevalence of the East Asian monsoon and the uplift of the Hengduan Mountains (HDM). In summary, our study provides novel insights into the plastome evolution, phylogenetic relationships, taxonomic framework and evolution of genus Sanicula.
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spelling doaj.art-2e0f1b731c934b9a991ff5186bafd22d2024-03-05T16:24:45ZengBMCBMC Plant Biology1471-22292024-01-0124112010.1186/s12870-024-04750-0Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analysesBo-Ni Song0Chang-Kun Liu1An-Qi Zhao2Rong-Ming Tian3Deng-Feng Xie4Yu-Lin Xiao5Huai Chen6Song-Dong Zhou7Xing-Jin He8Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityCAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of SciencesKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan UniversityAbstract Background The genus Sanicula L. is a unique perennial herb that holds important medicinal values. Although the previous studies on Sanicula provided us with a good research basis, its taxonomic system and interspecific relationships have not been satisfactorily resolved, especially for those endemic to China. Moreover, the evolutionary history of this genus also remains inadequately understood. The plastid genomes possessing highly conserved structure and limited evolutionary rate have proved to be an effective tool for studying plant phylogeny and evolution. Results In the current study, we newly sequenced and assembled fifteen Sanicula complete plastomes. Combined with two previously reported plastomes, we performed comprehensively plastid phylogenomics analyses to gain novel insights into the evolutionary history of this genus. The comparative results indicated that the seventeen plastomes exhibited a high degree of conservation and similarity in terms of their structure, size, GC content, gene order, IR borders, codon bias patterns and SSRs profiles. Such as all of them displayed a typical quadripartite structure, including a large single copy region (LSC: 85,074–86,197 bp), a small single copy region (SSC: 17,047–17,132 bp) separated by a pair of inverted repeat regions (IRs: 26,176–26,334 bp). And the seventeen plastomes had similar IR boundaries and the adjacent genes were identical. The rps19 gene was located at the junction of the LSC/IRa, the IRa/SSC junction region was located between the trnN gene and ndhF gene, the ycf1 gene appeared in the SSC/IRb junction and the IRb/LSC boundary was located between rpl12 gene and trnH gene. Twelve specific mutation hotspots (atpF, cemA, accD, rpl22, rbcL, matK, ycf1, trnH-psbA, ycf4-cemA, rbcL-accD, trnE-trnT and trnG-trnR) were identified that can serve as potential DNA barcodes for species identification within the genus Sanicula. Furthermore, the plastomes data and Internal Transcribed Spacer (ITS) sequences were performed to reconstruct the phylogeny of Sanicula. Although the tree topologies of them were incongruent, both provided strong evidence supporting the monophyly of Saniculoideae and Apioideae. In addition, the sister groups between Saniculoideae and Apioideae were strongly suggested. The Sanicula species involved in this study were clustered into a clade, and the Eryngium species were also clustered together. However, it was clearly observed that the sections of Sanicula involved in the current study were not respectively recovered as monophyletic group. Molecular dating analysis explored that the origin of this genus was occurred during the late Eocene period, approximately 37.84 Ma (95% HPD: 20.33–52.21 Ma) years ago and the diversification of the genus was occurred in early Miocene 18.38 Ma (95% HPD: 10.68–25.28 Ma). Conclusion The plastome-based tree and ITS-based tree generated incongruences, which may be attributed to the event of hybridization/introgression, incomplete lineage sorting (ILS) and chloroplast capture. Our study highlighted the power of plastome data to significantly improve the phylogenetic supports and resolutions, and to efficiently explore the evolutionary history of this genus. Molecular dating analysis explored that the diversification of the genus occurred in the early Miocene, which was largely influenced by the prevalence of the East Asian monsoon and the uplift of the Hengduan Mountains (HDM). In summary, our study provides novel insights into the plastome evolution, phylogenetic relationships, taxonomic framework and evolution of genus Sanicula.https://doi.org/10.1186/s12870-024-04750-0ApiaceaeSaniculaPlastomeDNA barcodesPhylogenyDivergence time
spellingShingle Bo-Ni Song
Chang-Kun Liu
An-Qi Zhao
Rong-Ming Tian
Deng-Feng Xie
Yu-Lin Xiao
Huai Chen
Song-Dong Zhou
Xing-Jin He
Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
BMC Plant Biology
Apiaceae
Sanicula
Plastome
DNA barcodes
Phylogeny
Divergence time
title Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
title_full Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
title_fullStr Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
title_full_unstemmed Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
title_short Phylogeny and diversification of genus Sanicula L. (Apiaceae): novel insights from plastid phylogenomic analyses
title_sort phylogeny and diversification of genus sanicula l apiaceae novel insights from plastid phylogenomic analyses
topic Apiaceae
Sanicula
Plastome
DNA barcodes
Phylogeny
Divergence time
url https://doi.org/10.1186/s12870-024-04750-0
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