Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae

Abstract Background Chloranthaceae is a pantropical family of flowering plants distributed mainly across Central and South America, East Asia, and the Pacific, encompassing approximately 73 species belonging to four extant genera—Ascarina, Chloranthus, Hedyosmum, and Sarcandra. As one of the most an...

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Main Authors: Peng-Wei Li, Yong-Bin Lu, Xin-Mei Qin, Qiang Zhang
Format: Article
Language:English
Published: BMC 2025-04-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06586-8
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author Peng-Wei Li
Yong-Bin Lu
Xin-Mei Qin
Qiang Zhang
author_facet Peng-Wei Li
Yong-Bin Lu
Xin-Mei Qin
Qiang Zhang
author_sort Peng-Wei Li
collection DOAJ
description Abstract Background Chloranthaceae is a pantropical family of flowering plants distributed mainly across Central and South America, East Asia, and the Pacific, encompassing approximately 73 species belonging to four extant genera—Ascarina, Chloranthus, Hedyosmum, and Sarcandra. As one of the most ancient lineages of extant angiosperms, Chloranthaceae holds substantial value in traditional medicine globally and offers major insights into the evolutionary history of flowering plants. However, phylogenetic relationships within this family remain partially resolved, and its origin continues to be debated. We here sequenced, assembled, annotated, and compared the chloroplast genomes (plastomes) of 22 Chloranthaceae species to investigate their plastome evolution and reconstructed the family’s phylogeny by using both plastome and nuclear ribosomal DNA (nrDNA). Additionally, we employed the divergence-extinction-cladogenesis model to infer the ancestral area and historical migration patterns of Chloranthaceae. Results Results The plastomes of Chloranthaceae exhibit a typical quadripartite structure, with genome sizes ranging from 157,449 bp to 159,218 bp and encoding 113 unique genes, including 17–18 genes duplicated in inverted repeat (IR) regions. Interestingly, the genus Hedyosmum demonstrated notable IR expansions, resulting in trnH GUG duplication in five species. A comparative analysis unveiled substantial variations in simple sequence repeats (SSRs) and tandem repeats across different species, whereas interspersed repeats remained relatively stable. Correlation analyses revealed positive correlations between plastome size and both IR length and SSR count. Furthermore, our phylogenetic reconstruction based on plastome and nrDNA (18 S-ITS1-5.8 S-ITS2-26 S) data provided robust support for the intergeneric relationships, confirming the monophyly of each genus and resolving long-standing uncertainties in the intrageneric relationships of Chloranthus and Hedyosmum. Notably, H. orientale, the sole Hedyosmum species found in Asia, was phylogenetically embedded within the genus, rather than occupying a basal position contrary to previous results. Our biogeographical reconstruction, incorporating both extant and fossil evidence, supports a Laurasian origin of Chloranthaceae and its subsequent dispersal to the tropics. Conclusion Conclusions This study provides the most comprehensive plastome-based phylogenomic analysis of Chloranthaceae to date, offering novel insights into its plastome evolution, resolving long-standing ambiguities in interspecific and phylogenetic relationships and reconstructing the probable biogeographic origin and historical migrations of this family. The proposed resources establish a robust framework for future evolutionary investigations within the realm of Chloranthaceae.
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spelling doaj-art-fa4e2a01453349539cb2064aa5a7bbfa2025-08-20T03:14:10ZengBMCBMC Plant Biology1471-22292025-04-0125111710.1186/s12870-025-06586-8Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of ChloranthaceaePeng-Wei Li0Yong-Bin Lu1Xin-Mei Qin2Qiang Zhang3Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of SciencesGuangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of SciencesGuangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of SciencesGuangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of SciencesAbstract Background Chloranthaceae is a pantropical family of flowering plants distributed mainly across Central and South America, East Asia, and the Pacific, encompassing approximately 73 species belonging to four extant genera—Ascarina, Chloranthus, Hedyosmum, and Sarcandra. As one of the most ancient lineages of extant angiosperms, Chloranthaceae holds substantial value in traditional medicine globally and offers major insights into the evolutionary history of flowering plants. However, phylogenetic relationships within this family remain partially resolved, and its origin continues to be debated. We here sequenced, assembled, annotated, and compared the chloroplast genomes (plastomes) of 22 Chloranthaceae species to investigate their plastome evolution and reconstructed the family’s phylogeny by using both plastome and nuclear ribosomal DNA (nrDNA). Additionally, we employed the divergence-extinction-cladogenesis model to infer the ancestral area and historical migration patterns of Chloranthaceae. Results Results The plastomes of Chloranthaceae exhibit a typical quadripartite structure, with genome sizes ranging from 157,449 bp to 159,218 bp and encoding 113 unique genes, including 17–18 genes duplicated in inverted repeat (IR) regions. Interestingly, the genus Hedyosmum demonstrated notable IR expansions, resulting in trnH GUG duplication in five species. A comparative analysis unveiled substantial variations in simple sequence repeats (SSRs) and tandem repeats across different species, whereas interspersed repeats remained relatively stable. Correlation analyses revealed positive correlations between plastome size and both IR length and SSR count. Furthermore, our phylogenetic reconstruction based on plastome and nrDNA (18 S-ITS1-5.8 S-ITS2-26 S) data provided robust support for the intergeneric relationships, confirming the monophyly of each genus and resolving long-standing uncertainties in the intrageneric relationships of Chloranthus and Hedyosmum. Notably, H. orientale, the sole Hedyosmum species found in Asia, was phylogenetically embedded within the genus, rather than occupying a basal position contrary to previous results. Our biogeographical reconstruction, incorporating both extant and fossil evidence, supports a Laurasian origin of Chloranthaceae and its subsequent dispersal to the tropics. Conclusion Conclusions This study provides the most comprehensive plastome-based phylogenomic analysis of Chloranthaceae to date, offering novel insights into its plastome evolution, resolving long-standing ambiguities in interspecific and phylogenetic relationships and reconstructing the probable biogeographic origin and historical migrations of this family. The proposed resources establish a robust framework for future evolutionary investigations within the realm of Chloranthaceae.https://doi.org/10.1186/s12870-025-06586-8BiogeographyIR expansionLaurasianPhylogenyPlastomeRepeat sequence
spellingShingle Peng-Wei Li
Yong-Bin Lu
Xin-Mei Qin
Qiang Zhang
Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
BMC Plant Biology
Biogeography
IR expansion
Laurasian
Phylogeny
Plastome
Repeat sequence
title Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
title_full Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
title_fullStr Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
title_full_unstemmed Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
title_short Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae
title_sort plastome phylogenomics unravels the evolutionary relationships and biogeographic history of chloranthaceae
topic Biogeography
IR expansion
Laurasian
Phylogeny
Plastome
Repeat sequence
url https://doi.org/10.1186/s12870-025-06586-8
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AT yongbinlu plastomephylogenomicsunravelstheevolutionaryrelationshipsandbiogeographichistoryofchloranthaceae
AT xinmeiqin plastomephylogenomicsunravelstheevolutionaryrelationshipsandbiogeographichistoryofchloranthaceae
AT qiangzhang plastomephylogenomicsunravelstheevolutionaryrelationshipsandbiogeographichistoryofchloranthaceae