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 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.

The Micromorphology and Its Taxonomic Value of the Genus Sanicula L. in China (Apiaceae)

“…In addition, the stomata in the lower epidermis of S. pengshuiensis was ovoid, while that in S. lamelligera was elliptical, so we considered them as two independent species. The previous molecular research also justified our micromorphological study [ 3 ]. Song et al performed phylogenetic analyses based on plastome data and found that S. tienmuensis and S. astrantiifolia had close relationship with weak supports and low resolutions, which made them difficult to distinguish [ 3 ].…”

“…Of those, nineteen species and five varieties are distributed in China, with eleven species and five varieties of them endemic [ 4 , 5 , 6 , 7 ]. The genus was considered as a taxonomically difficult group within Apiaceae and exhibited diversity in habits, leaves, inflorescences, fruits and rhizomes [ 2 , 3 ]. The plants of the genus mainly grow in grassy places on stream banks, rocky walls, alpine scrub, shady wet places, mixed forests on mountain slopes, bamboo forests, wet shady valleys and other habits [ 5 , 6 ] ( Figure 1 ).…”

Plastid phylogenomics contributes to the taxonomic revision of taxa within the genus Sanicula L. and acceptance of two new members of the genus

“…The genus comprises approximately 45 species that are widely distributed from East Asia to North America, with China and North America as two diversification centers ( Van et al., 2013 ; Li et al., 2023 ). Among them, nineteen species and five varieties are distributed in China and eleven species and five varieties are endemic ( Sheh and Phillippe, 2005 ; Pimenov, 2017 ; Xie et al., 2019 ; Li et al., 2023 ; Song et al., 2024 ). The most distinctive characteristic features of the genus are the fruits (mericarps) covered with scales, bristles, or hooked prickles, a rather prominent and persistent calyx, and two persistent styles that can easily distinguish it from other genera of Apiaceae ( Pryer and Phillippe, 1989 ; Calviño and Downie, 2007 ).…”

“…In most angiosperms, plastids are usually considered to be inherited from the maternal parent and have low nucleotide substitution rates ( Wicke et al., 2011 ; Wataru and Tsuneaki, 2023 ). Thus, the plastid genomes (plastomes) have been widely and successfully used for plant phylogenetic analyses ( Duminil et al, 2012 ; Miller et al, 2014 ; Razafimandimbison et al, 2014 ; Zhang et al, 2018 ; Schneider et al, 2021 ; Xu and Hong., 2021 ; Ji et al., 2022 ; Scatigna et al, 2022 ; Xiang et al, 2022 ; Baldwin et al, 2023 ; Fu et al, 2023 ), especially for those taxonomically controversial taxa within the family Apiaceae ( Gou et al., 2020 ; Ren et al., 2020 , 2022 ; Cai et al., 2022 ; Liu et al., 2022 ; Guo et al., 2023 ; Liu et al., 2023a ; Lei et al., 2022 ; Gui et al., 2023 ; Peng et al., 2023 ; Qin et al., 2023 ; Song et al., 2023 ; Tian et al., 2023 ; Song et al., 2024 ). For example, Song et al.…”

“…Therefore, plastomes also provided a promising window for studying the genus Sanicula. In the previously published studies ( Yang et al., 2022 ; Li et al., 2023 ; Song et al., 2024 ), researchers have used the plastomes data to investigate the phylogenetic positions of Sanicula members, which has significantly improved our understanding of this taxonomically confused group. However, sampling of this genus was limited and the interspecific relationships of some members were still unclear, such as S. giraldii H. Wolff and S. giraldii var.…”