Plastome evolution in the genus Sium (Apiaceae, Oenantheae) inferred from phylogenomic and comparative analyses
BMC Plant Biology volume 23, Article number: 368 (2023)
Sium L. (Apiaceae) is a small genus distributed primarily in Eurasia, with one species also occurring in North America. Recently, its circumscription has been revised to include 10 species, however, the phylogenetic relationships within its two inclusive clades were poorly supported or collapsed in previous studies based on nuclear ribosomal DNA ITS or cpDNA sequences. To identify molecular markers suitable for future intraspecific phylogeographic and population genetic studies, and to evaluate the efficacy of plastome in resolving the phylogenetic relationships of the genus, the complete chloroplast (cp) genomes of six Sium species were sequenced.
The Sium plastomes exhibited typical quadripartite structures of Apiaceae and most other higher plant plastid DNAs, and were relatively conserved in their size (153,029–155,006 bp), gene arrangement and content (with 114 unique genes). A total of 61–67 SSRs, along with 12 highly divergent regions (trnQ, trnG-atpA, trnE-trnT, rps4-trnT, accD-psbI, rpl16, ycf1-ndhF, ndhF-rpl32, rpl32-trnL, ndhE-ndhG, ycf1a and ycf1b) were discovered in the plastomes. No significant IR length variation was detected showing that plastome evolution was conserved within this genus. Phylogenomic analysis based on whole chloroplast genome sequences produced a highly resolved phylogenetic tree, in which the monophyly of Sium, as well as the sister relationship of its two inclusive clades were strongly supported.
The plastome sequences could greatly improve phylogenetic resolution, and will provide genomic resources and potential markers useful for future studies of the genus.
Sium L. is a small genus belonging to the tribe Oenantheae of Apiaceae subfamily Apioideae, which included 12 species in previous delimitation [1,2,3]. The major distribution center of the genus is Eurasia, where nine species occur (S. ventricosum (H.de Boissieu) L.S.Wang & M.F.Watson, S. latifolium L., S. medium Fisch. & C.A.Mey., S. ninsi Thunb., S. serra (Franch. & Sav.) Kitag., S. sisaroideum DC., S. sisarum L., S. suave Walter-it is also distributed in North America, and S. tenue Kom.). In sub-Saharan Africa, the genus has one species (S. repandum Welw. ex Hiern), while Sium burchellii (Hook. f.) Hemsl. and S. bracteatum (Roxb.) Cronk are endemic to the island of Saint Helena. The genus compassed species that often live in moist to aquatic habitats, and characterized by glabrous throughout, fascicled, fusiform or fibrous roots, simple pinnate leaves with sessile pinnae, long and reflexed styles, fruits with prominent and corky-thickened ribs .
Some species of Sium are used as herbal medicines in Chinese folk remedies . They are rich in essential oils , and can be used for dispelling wind-cold, relieving headache and lowering blood pressure . The thickened roots of Sium sisarum are rich in carbohydrates, and served as food before the potato was introduced [7, 8]. Furthermore, Sium suave is often sold in medicinal markets as an adulterant of “Gao-ben” .
The circumscription of Sium and its infrageneric phylogenetic relationships have been controversial. For example, members of the traditionally delimited Berula and Sium have long been considered closely related and sometimes even synonymous . Moreover, the relationship between the African and the non-African members of Sium is unclear . In recent years, several molecular phylogenetic studies have been conduted on Sium, and the taxonomic status of some species were resolved. Among them, Pimpinella crispulifolia H.de Boissieu was transferred into the Sium based on morphological and molecular analysis , and S. serra and S. ventricosum were recognized as belonging to the genus Sium . Furthermore, the comprehensive revision of the tribe Oenantheae [12, 13], along with the molecular phylogenetic analysis of Sium and related genera [1, 14], showed that the genus Sium, as previously circumscribed (with 12 species), was shown to be polyphyletic. Its three species (S. repandum, S. burchellii and S. bracteatum) outside of Eurasia (from sub-Saharan African/Saint Helena), together with Berula (Africa, Eurasia and North America) and Afrocarum (Africa), formed a strongly supported clade (Berula s.l.). Berula s.l. has been recognized at the generic level and these African/Saint Helena species were thus transferred into the genus Berula. The remaining species constituted the Sium s.s., including the northern Holarctic clade (whose members generally occur in the northern Holarctic) and the southern Palearctic clade (whose members are distributed in the Palearctic, usually farther south than those of the northern Holarctic clade). However, the phylogenetic relationships between the two inclusive clades were poorly supported in the ITS trees [1, 11], or they comprised two branches of a five-way polytomy in the cpDNA (rps16-trnK) analysis . Therefore, it is necessary to use more effective molecular markers or genomic data to investigate the phylogenetic relationship between the two clades.
Plastomes can provide valuable information for taxonomy and phylogeny, and have proven to be a powerful tool for exploring phylogenetic relationships [15, 16]. It have been applied to the comparative analysis and phylogenetic reconstruction of Apiaceae, in which the genome structure was characterized and some contentious phylogenetic relationships have been resolved [17,18,19,20,21,22,23,24]. Furthermore, highly divergent regions and simple sequence repeats (SSRs) obtained from plastome sequences can be used as efficient molecular markers for species delimitation, as well as population genetics .
In this study, the complete chloroplast (cp) genomes of six Sium species were sequenced, characterized and compared. We aimed to: (1) analyze the global features and structural patterns of Sium cp genomes; (2) identify simple sequence repeats (SSRs) and hotspot regions within Sium; (3) evaluate the efficacy of the whole cp genome in resolving the relationships within the genus, and compared with the results of ITS analysis. This is the first comprehensive analysis on cp genomes of the genus Sium, the results of which will provide genetic resources and molecular markers for future studies of this genus.
Characteristics of Sium plastomes
The seven complete cp genomes of Sium range in length from 153,029 bp (S. ventricosum) to 155,006 bp (S. ninsi), with the GC content identically 37.40% (Table 1). All the plastomes display a typical quadripartite structure, compose of a LSC region of 84,111–85,036 bp, a SSC region of 17,092–18,789 bp, and two inverted repeats (IRa and IRb) each of 24,970–26,472 bp (Fig. 1). They harbor 132 genes with the same arrangement order, including 87 protein-coding genes, 8 rRNA genes, and 37 tRNA genes. Most genes have a single copy, while 7 protein-coding genes (ndhB, rpl2, rpl23, rps7, rps12, ycf2 and ycf15), 7 tRNA genes (trnA-UGC, trnI-GAU, trnI-CAU, trnL-CAA, trnN-GUU, trnR-ACG and trnV-GAC), and four rRNA genes (rrn16, rrn23, rrn4.5 and rrn5) are duplicated in the IR regions (Fig. 1, Table S1). Of the 114 unique genes, 18 genes (including 12 protein-coding genes and 6 tRNA genes) have introns, with 16 genes (atpF, ndhA, ndhB, petB, petD, rpl2, rpl16, rpoC1, rps12, rps16, trnA-UGC, trnG-UCC, trnI-GAU, trnK-UUU, trnL-UAA and trnV-UAC) having one intron and two genes (ycf3 and clpP) having two introns. The two individuals of S. suave present minor difference in length, with 154,642 bp (S. suave 1) and 154,676 bp (S. suave 2). In general, the plastomes of Sium are highly identical in their structural organization, gene order and gene content.
Sequence repeats analysis
A total of 452 SSRs are identified in the seven Sium cp genomes (Fig. 2 and Table S2). The number of SSRs discovered in each species range from 61 (S. medium) to 67 (S. suave) (Fig. 2A). They are mainly located in LSC (265 SSRs, 58.63%) or IR region (111 SSRs, 24.56%), and only a minority are occurred in the SSC region (76 SSRs, 16.81%) (Fig. 2B). Among which, mono-nucleotide, di-nucleotide, tri-nucleotide, tetra-nucleotide, and penta-nucleotide repeats are detected in all species, while hexa-nucleotides SSRs (CCTATA) are only found in S. ventricosum, S. tenue and S. ninsi (Fig. 2C). The most abundant repeats are mono-nucleotide, which accounts for 50.00–63.93% of the total, followed by di-nucleotide repeats (20.21–26.87%), tetra-nucleotide repeats (6.56–19.70%), tri-nucleotide repeats (1.64–6.25%), and penta-nucleotide repeats have the least amount (1.61–4.48%). Meanwhile, the majority of SSRs are the A/T type (80.30–85.25%).
Comparative genomic analysis
The aligned cp genomes of six Sium species result in a matrix of 158,319 bp, and show high sequence similarity (99.20–99.96%). In which, 2630 variable sites and 1245 parsimony informative sites are included. The divergence levels of the noncoding and single-copy regions (LSC and SSC) are higher than that of the coding and IR regions, respectively (Fig. 3). At the genome level, the sequence divergence among the six Sium species range from 0.0004 to 0.0080, with an average of 0.0060. Furthermore, the two species endemic to China (S. ventricosum and S. crispulifolium) show the sequence divergence of 0.0060, and the largest sequence divergence value is observed between S. crispulifolium and S. medium (0.0080).
The sliding window analyses across the seven plastomes show that the nucleotide diversity (Pi) range from 0.0000 to 0.0327 (Fig. 4). A total of 12 regions (trnQ, trnG-atpA, trnE-trnT, rps4-trnT, accD-psbI, rpl16, ycf1-ndhF, ndhF-rpl32, rpl32-trnL, ndhE-ndhG, ycf1a and ycf1b) are recognized as hotspot regions with nucleotide diversity > 0.015. Of those, six regions are located in the LSC, and six were in the SSC region. The NJ trees show that all these regions could identify Sium species separately or jointly (Figures S1 and S2). The primers are designed for the 12 variable markers (Table S3).
The expansion and contraction of the junction regions are analyzed for the six Sium species, and no significant IR length variation is detected (Fig. 5). The genes rps19, rpl2, ycf1, ndhF and trnH are present at the junction of the LSC/IRb, IRb/SSC, SSC/IRa and IRa/LSC borders. In all plastomes, the LSC/IRb boundary is located within the rps19 gene, with part of it (58–79 bp) duplicated in the IRa. Similarly, the SSC/IRa junction are located in the ycf1 gene across all species, resulting in the presence of ψycf1 in the IRb. There are two copies of the rpl2 genes located in the IR regions (IRa and IRb), which is 117–139 bp away from the LSC/IR junction, while the trnH gene is just located at the junction of LSC/IRa region in all plastomes. The ndhF gene of S. ninsi, S. tenue and S. ventricosum are completely located in the SSC region, which extends into the IRb region by about 7–39 bp in other species. These variations at boundary regions lead to the length variation in the cp genomes of Sium.
Using the complete cp genome sequences, phylogenetic relationships among the major clades of Apioideae, as well as six Sium species are inferred. The phylogenies estimated using ML and BI analyses are well-resolved and fully consistent with one another (Fig. 6). In all analyses, the monophyly of Sium is recovered with strong support (bootstrap value, BS = 100, PP = 1.00). Within Sium, two monophyletic sister clades are recognized with high support (BS = 100, PP = 1.00). Clade I includes two species distributed in the northern Holarctic [1, 14]: central Asiatic S. medium is sister group to the clade of eastern Asiatic-North American S. suave. The remaining species of the genus constitute the Clade II, in which the two species endemic to China (S. ventricosum and S. crispulifolium) ally together, and comprise a sister group relationship to the group of S. ninsi and S. tenue. The ITS and plastome trees produce consistent topologies for Sium species (Figure S3).
In this study, we assembled and annotated the complete plastid genome sequences of six Sium species for the first time. Having a range of 153,029–155,006 bp, the genome sizes of Sium fell within the typical size range of Apiaceae plastomes [17,18,19,20,21,22,23,24,25]. Furthermore, all plastomes are typical of Apiaceae and most other angiosperms plastid DNAs in terms of structural organization, gene arrangement and content. The cp genomes of Sium species had an average GC content of 37.40%, similar to those previously published Apiaceae genomes [22, 23]. Moreover, the GC contents in LSC and SSC regions were significantly lower than those in the IR region, as the rRNA genes with high GC content located in IR regions. In Apiaceae, the expansion and contraction of the IR region, and the introgression of mitochondrial DNA into the plastid genome have been previously reported for some species [25,26,27,28,29,30]. In the present study, however, no significant IR length variation was detected among Sium plastomes, showing that plastome evolution was conserved within this genus.
To better resolve relationships among closely related species, great efforts have been made to identify more variable chloroplast regions [31,32,33]. Across Apiaceae lineages, the rpl32-trnL, trnE-trnT, ndhF-rpl32, rps16-trnQ and trnT-psbD intergenic spacers are among the most fast-evolving loci, while the trnD-trnY-trnE-trnT combined region presents the greatest number of potentially parsimony informative characters . In which, rps16-trnQ, rpl32-trnL intergenic spacers and rps16 introns have previously been considered useful in resolving low-level relationships of Apiaceae [34,35,36,37,38]. In addition to these loci, we found that a total of nine regions held a relatively higher Pi values for Sium: trnQ, trnG-atpA, rps4-trnT, accD-psbI, rpl16, ycf1-ndhF, ndhE-ndhG, ycf1a and ycf1b. Although some regions yielded species relationships that differed from the genomic results, all Sium species could be successfully identified on the neighbor-joining trees. Therefore, these regions can be used as lineage-specific DNA barcodes in future plant identification and speciation studies in Sium. SSRs play an important role as molecular markers in plant population genetics, evolutionary and ecological studies due to their high levels of mutation rates and polymorphism . In this study, we identified 61 to 67 SSRs in seven Sium plastomes, which will be conducive to the assessment of genetic differentiation within and among populations .
In recent years, several molecular studies on tribe Oenantheae and the genus Sium, based on nuclear rDNA ITS and few cpDNA sequences, have been carried out [1, 12,13,14]. In all of these studies, Sium is resolved as a polyphyletic group, as its African and Saint Helena members (S. repandum, S. bracteatum and S. burchellii), along with the monotypic African Afrocarum, were nested within Berula forming the Berula s.l. clade. These four African/Saint Helena species have been transferred into the genus Berula . The remaining nine species of Sium constituted the Sium s.s., and consisted of two clades: the northern Holarctic clade (S. latifolium, S. medium and S. suave) and the southern Palearctic clade (included S. ventricosum, S. ninsi, S. serra, S. sisaroideum, S. sisarum and S. tenue). In all analyses, the monophyly of each of the two clades is strongly supported, however, their sister group relationship was poorly supported or collapsed in previous studies [1, 11, 14]. With the use of complete cp genome sequences, a highly consistent topology was recovered, the monophyly of the northern Holarctic clade and the southern Palearctic clade, and their sister relationship were strongly supported. Sium crispulifolium was a poorly known species endemic to China, and it was initially described under Pimpinella as P. crispulifolia H.de Boissieu . However, this placement was not certain because the type specimen has no ripe fruits. Recently, based on molecular affinity, and morphological similarity to Sium (e.g., fascicled root, long and reflexed styles, conspicuous calyx teeth, and fruits with corky-thickened ribs), it was transferred into the Sium . Thus, the circumscription of Sium was expanded to accommodate 10 species. Sium ventricosum is an aquatic and dwarf plant endemic to high montane regions in southwest of China , which has been variously treated as species of Apium, Chamaesium, Sium, and Sinocarum [41,42,43]. In the present analysis, Sium ventricosum and S. crispulifolium constituted a well-supported sister group, and allied strongly with two other eastern Asia representatives (S. tenue and S. ninsi) within Clade II. Therefore, phylogenomic analysis further confirmed that they belong to the genus Sium. The phylogenetic positions of other Sium species were generally consistent with those inferred by previous studies [1, 11, 14], but with higher support.
In this study, the cp genomes of six Sium species were analyzed and compared. The results revealed that the Sium plastomes are conserved in structural organization, gene order and content. The SSRs and hotspot regions identified can be used as molecular markers in the future intraspecific diversity study of Sium. Furthermore, our study showed that plastome sequences could greatly improve phylogenetic resolution. Overall, the complete plastome sequences reported herein enriched the genomic information available for Sium.
Taxon sampling and genome sequencing
A total of seven accessions, representing six Sium species were sampled for analysis (Table 1). The collection and voucher information are provided in Table 1. All samples were initially identified by the first author, then their respective ITS sequences were extracted from sequenced genomes and compared with that of Spalik et al.  for confirmation (the accession number for comparison are as follows: S. ninsi, DQ005678; S. suave, DQ005695; S. ventricosum, DQ005665; S. tenue, DQ005706; S. medium, DQ005674). DNA extractions were conducted using the Plant Genomic DNA Kit from Tiangen Biotech (Beijing) Co., Ltd., China. According to the manufacturer’s instructions, the total DNA was fragmented ultrasonically and used for 350-bp insert libraries construction. All of the genomic data were sequenced using the Illumina platform at Novogene (Beijing, China), with the paired-end reads 2 × 150 bp.
Assembling and annotation
Raw sequence reads were quality trimmed using Trimmomatic v.0.36 . Remaining high-quality reads were assembled de novo into contigs in SPAdes v3.6.1 . and GetOrganelle v1.6.4  with default settings. Contigs were connected with the help of Bandage version 0.8.1 , and manually checked when necessary. The cp genomes were annotated using CpGAVAS2 , and further manually adjusted in Geneious v.9.0.5  according to comparisons with the plastome of Tiedemannia filiformis subsp. greenmannii (Mathias & Constance) M.A. Feist & S.R. Downie . The tRNA genes were confirmed with tRNA scan-SE . The circular plastid genome maps were drawn using the Organellar GenomeDRAW . The seven Sium cp genomes and ITS sequences were submitted to GenBank (accession numbers for plastomes and ITS are OP234514–OP234520 and OR116133-OR116139, respectively).
Simple repeat sequence analysis
The simple sequence repeats (SSRs) of Sium plastomes were identified with MISA . Thresholds for the minimum number of repeats were 10, 5, 4, 3, 3, and 3 for mono-, di-, tri-, tetra-, penta-, and hexa nucleotides, respectively.
Genome comparison and analysis
The mVISTA program was used to evaluate the variability of the seven complete cp genome sequences under Shuffle-LAGAN mode , using S. crispulifolium as a reference. To determine the nucleotide diversity (Pi) among the cp genomes of Sium, the sliding window analysis was conducted using DnaSP v.6.10 , with a step size of 200 bp and a window length of 800 bp. The primers for amplifying the highly variable regions were designed using Primer Premier 6 software (Premier, Vancouver, Canada). We also compared junction sites of LSC-IRa/b and SSC-IRa/b with IRscope  to detect IR expansion or contraction in the genomes of the Sium species.
In total, forty-one cp genomes, representing the taxa from major clades of Apioideae and seven newly obtained taxa, were used in the phylogenetic analysis. Two Chamaesium taxa were selected as outgroup because the genus holds a sister-group relationship to all other apioid genera, excluding those of its most early-diverging branches [56, 57]. Fourthermore, the ITS sequences of the above taxa were analyzed for comparison with the genomic results. All sequences were aligned using the MAFFT v 7.017 , with the Q-INS-I algorithm , and manually adjusted where necessary using the BioEdit sequence alignment editor . Maximum likelihood (ML) analysis was conducted using RAxML version 8.1.11  using the GTR + G substitution model, with 1000 bootstrap replicates; other parameters were used as the default settings. Bayesian inference (BI) analysis was carried out with MrBayes version 3.2.3 . Four Markov chains starting with a random tree were run simultaneously for 1,000,000 generations, sampling trees at every 1000th generation. Convergence was assessed by examining the average standard deviation of split frequencies (ASDF) < 0.01. Trees from the first 25% were discarded as burn-in, and the remaining trees were used to build the fifty-percent majority-rule consensus tree and calculate the posterior probability (PP).
To verify the ability of highly divergent regions to identify Sium species, we performed phylogenetic analysis on these regions separately or jointly using MEGA 7.0. Neighbor-Joining (NJ) trees were calculated according to the Kimura 2-parameter (K2P) model using a bootstrap test with 1000 replicates.
Availability of data and materials
The seven plastomes generated in this study are available in GenBank of the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov; accession numbers are OP234514-OP234520; see Table 1); Voucher specimens are deposited in KUN and PE,and collection information was listed in Table 1. Raw sequence reads can be accessed by SRR21700072 for Sium crispulifolium_LZ1523, SRR21700479 for Sium medium_SCSB-SHI-2006220, SRR21707307 for Sium ninsi_Miyoshi Furuse 51,348, SRR21707790 for Sium suave_Chen Yaodong 571, SRR21721062 for Sium suave_S3, SRR21721663 for Sium tenue_lilan668, and SRR21732700 for Sium ventricosum_LZ20160686.
Average standard deviation of split frequencies
Large single copy region
Small single copy region
Simple sequence repeats
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We are grateful to Prof. Hua Peng for his valuable suggestions.
This work was supported by the National Natural Science Foundation of China (no. 31960048 and 31872649), the Ten Thousand Talents Program of Yunnan (YNWRQNBJ-2019–208), the department of Science and Technology of Yunnan Province (202201AT070118), the Hundred Talents Program of Kunming Medical University (no. 60118260127) and Gaoligong Mountain, Forest Ecosystem, Observation and Research Station of Yunnan Province (no. 202205AM070006).
Ethics approval and consent to participate
The Chen Yaodong 571 and Miyoshi Furuse 51348 are supplied by Herbarium, Institute of Botany Academia Sinica (PE), the lilan668 and SCSB-SHI-2006220 are supplied by Herbarium, Kunming Institute of Botany, Chinese Academy of Sciences (KUN), and the S3, LZ20160686 and LZ1523 were collected by the authors and deposited in Kunming Medical University. All materials were identified by Jing Zhou. The collection of plant material and use comply with relevant institutional, national, and international guidelines and legislation. This article does not contain any studies with human participants or animals and did not involve any endangered or protected species.
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Neighbor-Joining trees constructed for the 12 variable regions. A. ndhE-ndhG; B. ndhF-rpl32; C. rpl16; D. rpl32-trnL; E. rps4-trnT; F. trnE-trnT; G. trnG-atpA; H. trnQ; I. ycf1a; J: ycf1b; K. ycf1-ndhF; L. accD-psbI.
Neighbor-Joining tree constructed for the combined 12 variable regions.
Phylogenetic relationships of Sium species inferred from Bayesian Inference (BI) and Maximum Likelihood (ML) analyses of the ITS sequences. Bootstrap values (BS) and posterior probabilities (PP) are shown next to the branches. – indicated that the branch has no support value from BI analysis.
List of genes found in the Sium chloroplast genome.
More detail of SSRs in Sium species.
Primers for PCR amplification of the 12 variable regions among the seven Sium taxa.
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Zhou, J., Niu, J., Wang, X. et al. Plastome evolution in the genus Sium (Apiaceae, Oenantheae) inferred from phylogenomic and comparative analyses. BMC Plant Biol 23, 368 (2023). https://doi.org/10.1186/s12870-023-04376-8