Plastome phylogenomics unravels the evolutionary relationships and biogeographic history of Chloranthaceae

质体基因组系统发育学揭示了金粟兰科植物的进化关系和生物地理历史

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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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