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Research Article
Morphological and molecular evidence gives insight into the taxonomic position of Peucedanum pubescens (Apiaceae, Selineae)
expand article infoJiao-Jiao Deng, Chang-Kun Liu, Song-Dong Zhou, Xing-Jin He
‡ Sichuan University, Sichuan, China
Open Access

Abstract

In this study, morphological and molecular evidences were combined to determine the taxonomic position of Peucedanum pubescens Hand.-Mazz. Morphologically, Peucedanum pubescens is similar to the species of the genus Ligusticopsis in having fibrous remnant sheaths at the stem base, pinnate and linear coexisted bracts, strongly compressed dorsally mericarps, filiform median and lateral ribs, winged marginal ribs, numerous vittae in each furrow and commissure, but can also be easily distinguished from members of Ligusticopsis by its hispid fruit and linear-lanceolate bracteoles. Molecular phylogenetic analyses based on the single-copy protein-coding sequences (CDS) of plastomes and internal transcribed space (ITS) region showed that Peucedanum pubescens nested in the genus Ligusticopsis. As both morphological and molecular data supported the inclusion of Peucedanum pubescens within Ligusticopsis, the species is here transferred and the new combination, Ligusticopsis pubescens (Hand.-Mazz.) J.J.Deng, C.K.Liu & X.J.He, made.

Keywords

Apiaceae, Ligusticopsis pubescens, new combination, Peucedanum pubescens

Introduction

Peucedanum sensu lato was previously characterized by dorsally compressed mericarps with slightly prominent dorsal ribs, narrowly winged lateral ribs, as well as a broad commissure (Sheh 1992; Spalik et al. 2004; Sheh and Watson 2005). As such it was one of the largest genera of Apiaceae, comprising 100–120 species with 33 endemics to the territory of China, and with a distribution in Eurasia, South Africa, and sometimes Australia (Spalik et al. 2004; Sheh and Watson 2005; Cieśla et al. 2009). However, Peucedanum sensu lato has been a taxonomically confusing genus due to its great heterogeneous characteristics (Solov’eva et al. 1985; Reduron et al. 1997; Downie et al. 2000, 2010; Winter et al. 2008; Zhou et al. 2014), exhibiting a wide variety of life forms, leaf and fruit structures, and chemical compositions (Shneyer et al. 2003). Moreover, several molecular phylogenetic studies based on DNA fragments and plastomes indicated that Peucedanum sensu lato was not a monophyletic group (Downie et al. 2000; Spalik et al. 2004; Valiejo-Roman et al. 2006; Feng et al. 2009; Zhou et al. 2009, 2020; Liu et al. 2022). Consequently, the circumscription of the genus has been greatly reduced with Peucedanum sensu stricto, recognized by ternate leaves, linear-subulate or filiform bracteoles, one vitta in each furrow and two vittae on commissure in mericarp (Kadereit and Bittrich 2018) and several members of Peucedanum sensu lato were separated to restitute or establish genera or transfer into other genera (Reduron et al. 1997; Winter et al. 2008; Ostroumova et al. 2016; Pimenov et al. 2016; Pimenov 2017). However, the previous studies mainly focused on those species distributed in Europe and South Africa, and the taxonomic position of Chinese endemic species of this genus was still unresolved.

Ligusticopsis Leute was described by Leute in 1969 with Ligusticopsis rechingeriana Leute as its type species. The taxonomy of genus has been controversial since its establishment, due to its close morphology to Ligusticum (Zhou et al. 2008, 2009; Sun et al. 2010); e.g. Flora Reipublicae Popularis Sinicae and Flora of China treated Ligusticopsis as the synonym of Ligusticum and “Ligusticum in the broad sense”, respectively (Sheh 1992; Sheh and Watson 2005), whereas the genus was recognized by Pimenov et al. (2001, 2003). Recently, a phylogenetic study based on morphological and molecular data confirmed the monophyly of Ligusticopsis and nine “true species of Ligusticopsis” were recognized (Li et al. 2022); the members of the genus are characterized by the following diagnostic characters: stem base clothed in fibrous remnant sheaths, pinnate bracts, pinnate bracteoles longer than rays of umbellule, mericarps strongly compressed dorsally, median and lateral ribs filiform or keeled, marginal ribs winged, and numerous vittae in each furrow and commissure.

Peucedanum pubescens Hand.-Mazz. (1933: 728) was described based on a collection (E00002620) from Yunnan, China, and was an endemic species to China (Sheh and Watson 2005; Pimenov 2017). Due to dorsally compressed mericarps with slightly prominent dorsal ribs and narrowly winged lateral ribs, P. pubescens was recognized as a member of Peucedanum sensu lato (Handel-Mazzetti Heinrich 1933). However, after examination of the type specimen and protologue, field observation, and morphological and micro-morphological research into it, we found this species was characterized by stem base clothed in fibrous remnant sheaths, pinnate leaves, linear and pinnate coexisted bracts, strongly dorsally compressed fruits, numerous vittae in each furrow and commissure, and these features are significantly similar to members of Ligusticopsis. To determine the taxonomic position of Peucedanum pubescens, we performed morphological and molecular analyses.

Materials and methods

Morphological observation

The morphological features of Peucedanum pubescens were observed in field. Then, mericarp of this species was observed and photographed using a stereomicroscope, Nikon SMZ 25 (Japan). Furthermore, morphological diagnoses of nine “true species of Ligusticopsis” were obtained from type specimens from K, P, E, WU, BM, GH, KUN, and HNWP, Flora of China (Sheh and Watson 2005), and analysis performed by Li et al. (2022). The Herbarium code refers to Thiers (2015).

DNA extraction, ITS amplifying and sequencing

Total genomic DNA was extracted from silica-dried leaves with plant genomic DNA kit (Cwbio Biosciences, Beijing, China). The universal primers ITS4 (5’-TCC TCC GCT TAT TGA TAT GC-3’) and ITS5 (5’-GGA AGT AAA AGT CGT AAC AAG G-3’, White et al. 1990) were used to amplify the entire internal transcribed sequences (ITS). Amplification was undertaken using a volume of 30 µl with 15 µl 2 × Taq MasterMix (CWBIO, China), 10 µl ddH2O, 1.5 µl forward primer, 1.5 µl reverse primer, and 2 µl total DNA. The amplification of the ITS region was obtained by initial denaturation for 3 min at 94 °C, followed by 30 cycles of 45 s at 94 °C, 70 s at 54 °C, and 90 s at 72 °C, and then a final extension of 10 min at 72 °C. All PCR products were separated using a 1.5% (w/v) agarose TAE gel and sent to Sangon (Shanghai, China) for sequencing.

Plastome sequencing and assembly

The extracted total DNA was fragmented into 400 bp to construct the pair-end library, following the manufacturer’s protocol (Illumina, San Diego, CA, USA). The DNA libraries were sequenced on the Illumina NovaSeq platform at Personalbio (Shanghai, China). Quality control of the raw reads was performed using fastP v0.15.0 (-n 10 and -q 15) (Chen et al. 2018), produced at least 5GB clean reads per species. De novo genome assembly from the clean data was accomplished utilizing NOVOPlasty v2.6.2 (Dierckxsens et al. 2017), with a kmer length of 39 bp and a sequence fragment of the rbcL gene from Ligusticopsis brachyloba (Franch.) Leute (Genebank no. MN204661) as the seed sequence. The assembled complete plastome was annotated initially by using PGA (Qu et al. 2019) and then examined using Geneious v9.0.2 (Kearse et al. 2012).

Phylogenetic analyses

To confirm the phylogenetic position of Peucedanum pubescens, phylogenetic trees were reconstructed based on single-copy protein-coding sequences (CDS) of 34 plastomes and 36 ITS sequences (Table 1). Chamaesium mallaeanum Farille & S. B. Malla and Chamaesium viridiflorum (Franch.) Wolff ex Shan were selected as outgroups according to the result of a previous study (Li et al. 2022). Plastome CDs and ITS sequences were respectively aligned using MAFFT v7.221 (Katoh and Standley 2013), and then manually adjusted in MEGA7.0 (Kumar et al. 2016) to obtain plastome CDs and ITS datasets. The two alignments were subjected to Maximum-Likelihood (ML) analyses and Bayesian Inference (BI). For ML analyses, the software RAxML v8.2.8 (Stamatakis 2014) was used to construct the phylogenetic trees with the GTR+G+I model and 1000 bootstrap (BS) replicates. Bayesian inference (BI) analyses were conducted by MrBayes version 3.2.7 (Ronquist et al. 2012) with the best-fit substitution model (GTR+G+I) determined by Modeltest v3.7 (Posada and Crandall 1998). Markov Chain Monte Carlo (MCMC) search was performed for 1 × 106 generations, sampling every 100 generations. The first 25% of trees were discarded as burn-in and the remainder was used to generate the consensus tree. Results of phylogenetic analyses were visualized and edited in FigTree v1.4.2 (Rambaut and Drummond 2015).

Table 1.

Voucher details and GenBank accession numbers of taxa used in this study. A n-dash (–) indicates unavailable information.

Species Voucher information Locality GenBank accession number
Plastome ITS
Angelica cartilaginomarginata 13E-39-3, SZ2006071804 USA, NIH; China, Yunnan NC029393 EU647210
Angelic decursiva 13Q-02-1; v20060825 (SZ) Korea, Cheongju-si; China, Sichuan KT781591 EU418375
Angelica gigas 13E-39-3; SZ744110 USA, NIH; China, Sichuan NC029393 GU395156
Angelica laxifoliata –; 2006071804 (SZ) China, Sichuan; China, Yunnan NC040122 EU647210
Angelica nitida –; 2006080501 (SZ) China, Qinghai; China, Sichuan MF594405 EU418378
Bupleurum chinense –; C.Q. Feng China, Sichuan MN893666 EU001334
Bupleurum commelynoideum –; 2008082002 (SZ) China, Sichuan MN893666 GU269874
Chamaesium mallaeanum –; Strain NLM China, Sichuan; China, Xizang MT162552 KY74426
Chamaesium viridiflorum –; Strain HB China, Yunnan MN119373 KY744260
Glehnia littoralis –; SZ666775 China, Sichuan KU921430 GU395183
Hansenia forbesii –; SZ666939 China, Sichuan; China, Yunnan NC034645 GU390407
Hansenia oviformis –; F22 China, Sichuan MT843761 MT337430
Hansenia weberbaueriana –; J18091701 China, Sichuan MN049520 MN049520
Ligusticopsis brachyloba L081401 (SZ); L0814 (SZ) China, Chongqing MZ491174 MZ497218
Ligusticopsis capillacea RT2019100601 (SZ); XB China, Yunnan NC049051 MT974023
Ligusticopsis hispida RT2019100301 (SZ); L08110501 (SZ) China, Yunnan NC049052 OL600824
Ligusticopsis integrifolia RT2019100202 (SZ); L081003 (SZ) China, Yunnan NC049055 MZ497219
Ligusticopsis involucrata PC2018101905 (SZ); DB14 China, Yunnan NC049054 MT974014
Ligusticopsis modesta L081903 (SZ); L08190301 (SZ) China, Yunnan OL547615 OL600822
Ligusticopsis pubescens1 LCK2020817001 China, Yunnan ON872189 ON870396
Ligusticopsis pubescens2 LCK2020817002 China, Yunnan ON870397
Ligusticopsis pubescens3 LCK2020817003 China, Yunnan ON870398
Ligusticopsis rechingeriana L081103 (SZ); L081103 (SZ) China, Yunnan MZ491175 MZ497220
Ligusticopsis scapiformis RT2019082001 (SZ); CT9 China, Sichuan NC049057 MT974012
Ligusticopsis wallichiana LD081506 (SZ); LD08150601 (SZ) China, Xizang OL547616 OL600823
Ligusticum delavayi RT2019100301 (SZ); L08110501 (SZ) China, Yunnan NC049052 OL600824
Ligusticum jeholense –; LGB1 China, Liaoning; China, Beijing MT561037 KJ999437
Ligusticum sinense –; Ge131139 China, Sichuan; China, Guangdong NC038088 MH712648
Ligusticum tenuissimum 13I-08; JKTM-1-000065 Korea, Cheongju-si; Korea, Anyang-myeon NC029394 KP058314
Ligusticum thomsonii RT2019082301 (SZ); CJ (SZ) China, Sichuan MT409619 MT974009
Meeboldia yunnanensis –; G18071908 China, Yunnan MK993275 MN688997
Peucedanum ampliatum JQP19082505 (SZ); NASLQX022 China, Shanxi; – OK336475 JF977799
Peucedanum delavayi SZ YY 062105; YY062105 (SZ) EU418386 MT843765
Peucedanum japonicum LCK2020001 (SZ); sb1 China, Sichuan; – OK336477 EU224273
Peucedanum medicum LCK2020004 (SZ); SZ66876 China, Guangxi; – OK336473 HQ256686
Peucedanum praeruptorum –; SZ ZXM 001 MN016968 EU418383

Results

Morphological comparison

Peucedanum pubescens is similar to the species of Ligusticopsis in having fibrous remnant sheaths at the stem base (Fig. 3B), pinnate leaves (Fig. 3A, C–E), linear and pinnate coexisted bracts (Fig. 3F), strongly dorsally compressed fruits (Fig. 3G, H), numerous vittae in each furrow and commissure (Fig. 3H), but can be easily distinguished from the latter by the morphological characters shown in Table 2. In detail, Peucedanum pubescens is different from L. rechingeriana Leute, L. involucrata (Franch.) Lavrova and L. hispida (Franch.) Lavrova et Kljuykov in that P. pubescens has a triangular-ovate leaf blade in outline (Fig. 3C, D) (vs. oblong-ovate or lanceolate), obovate ultimate segments (Fig. 3C) (vs. ovate or linear), pinnate and linear coexist bracts (Fig. 3F) (vs. pinnate), linear-lanceolate bracteoles (vs. pinnate) (Fig. 3F), ovate to obovate mericarp shape (Fig. 3G) (vs. elliptic to ovate or elliptic), hispid mericarp surface (Fig. 3G, H) (vs. smooth) and 2–3 vittae in each furrow (Fig. 3H) (vs. 1–3). Peucedanum pubescens can be distinguished from L. integrifolia (H. Wolff) Leute, L. brachyloba and L. modesta (Diels) Leute in having linear-lanceolate bracteoles (Fig. 3F) (vs. pinnate and linear coexist or pinnate), hispid mericarp surface (Fig. 3G, H) (vs. smooth), ovate or obovate to orbicular mericarp shape (Fig. 3G) (vs. elliptic to ovate or elliptic) and 2–3 vittae in each furrow (Fig. 3H) (vs. 1–3 or 3–4 in each furrow). Peucedanum pubescens differs from L. capillacea Leute and L. scapiformis (H. Wolff) Leute in having triangular-ovate leaf blade in outline (Fig. 3C, D) (vs. oblong-ovate or oblong-lanceolate), pinnate and linear coexist bracts (Fig. 3F) (vs. pinnate), linear-lanceolate bracteoles (Fig. 3F) (vs. pinnate) and hispid mericarp surface (Fig. 3G, H) (vs. smooth). Peucedanum pubescens can be distinguished from L. wallichiana (DC.) Pimenov et Kljuykov in having pinnate and linear coexist bracts (Fig. 3F) (vs. pinnate), linear-lanceolate bracteoles (Fig. 3F) (vs. pinnate and linear coexist), ovate or obovate to orbicular mericarp shape (Fig. 3G) (vs. elliptic), hispid mericarp surface (Fig. 3G, H) (vs. smooth), 2–3 vittae in each furrow (Fig. 3H) (vs. 1–3) and filiform median rib shape (Fig. 3G, H) (vs. keeled).

Table 2.

Comparison of morphological characteristics between Peucedanum pubescens and the species of Ligusticopsis.

Characteristics P. pubescens L. rechingeriana L. involucrata L. hispida L. integrifolia L. brachyloba L. modesta L. capillacea L. scapiformis L. wallichiana
Stem (base) Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant Fibrous remnant
Leaves Pinnate, triangular-ovate Pinnate, oblong-ovate Pinnate, oblong-ovate Pinnate, lanceolate Pinnate, oblong-ovate Pinnate, triangular-ovate Pinnate, oblong-ovate Pinnate, oblong-ovate Pinnate, oblong-lanceolate Pinnate, broadly ovate
Ultimate segments of leaves Obovate Ovate Linear Linear Oblong-ovate or lanceolate Oblong-ovate or lanceolate Linear or lanceolate Obovate Ovate Linear
Bracts Pinnate and linear coexist Pinnate Pinnate Pinnate Pinnate and linear coexist Pinnate Pinnate Pinnate Pinnate Pinnate
Bracteoles linear-lanceolate Pinnate Pinnate Pinnate Pinnate and linear coexist Pinnate Pinnate Pinnate Pinnate Pinnate and linear coexist
Mericarp surface Hispid Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth Smooth
Mericarp shape ovate or obovate to orbicular Elliptic to ovate Elliptic Elliptic Elliptic to ovate Elliptic Elliptic to oblong Ovate Elliptic to ovate Elliptic
Calyx teeth Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous Conspicuous
Dorsal compression Strong Strong Strong Strong Strong Strong Strong Strong Strong Strong
Median rib shape Filiform Filiform Filiform Filiform Filiform Keeled Filiform Filiform Filiform Keeled
Vittae each furrow 2–3 1–3 1–3 1–3 1–3 2–3 3–4 1–3 1–4 1–3
Commissural vittae 6 6 6 6 6 6 8 6 4–6 6

Plastome feature of Peucedanum pubescens

The plastome of Peucedanum pubescens is a typically quadripartite structure, including a large single copy region (LSC), a small single copy region (SSC), and a pair of inverted repeat regions (IR) (Fig. 1). The overall size of plastome is 148,260 bp, and that of the LSC, IR, and SSC are 91,819 bp, 19,411 bp, and 17,619 bp, respectively. GC content analysis shows that the overall GC content is 37.0%, and the IR regions (43.8%) are higher than LSC (35.9%) and SSC (30.9%). The whole plastid genome contains 129 genes including 36 tRNAs, 8 rRNAs, and 85 protein-coding genes.

Phylogenetic analyses

The phylogenetic trees based on plastome CDs and ITS were given in Fig. 4 and Fig. 5, respectively. Both tree topologies strongly supported that Peucedanum pubescens nested in the genus Ligusticopsis (PP = 1.00 & BS = 100%; PP = 0.99 & BS = 88%). Although the phylogenetic position of this species could not be resolved in ITS tree, phylogenetic tree constructed based on plastome CDs showed that Peucedanum pubescens was sister to the clade that included the species L. rechingeriana (type species of the genus Ligusticopsis) and L. involucrata with high support (PP = 1.00 & BS = 99%).

Discussion

Peucedanum sensu stricto and Ligusticopsis both belong to the Selineae tribe of Apiaceae, and members of these two genera are similar in the dorsally compressed fruits with filiform dorsal ribs, and winged marginal ribs (Spalik et al. 2004; Sheh and Watson 2005; Li et al. 2022), but the former genus can be distinguished significantly from the latter by having ternate leaves, linear-subulate, caducous or lacking bracts, one vitta in a furrow and two vittae in commissure in mericarp (Kadereit and Bittrich 2018), while the latter can also be distinguished from the former by possessing pinnate leaves, pinnate bracts, numerous vittae in each furrow and in commissure (Li et al. 2022). Peucedanum pubescens is more similar to the genus Ligusticopsis in having pinnate leaves, linear and pinnate coexisting bracts, numerous vittae in each furrow and in commissure (Table 2), rather than Peucedanum sensu stricto. This result was further supported by the molecular phylogenetic analyses that Peucedanum pubescens nested in Ligusticopsis. As a result, Peucedanum pubescens is here transferred to Ligusticopsis as an independent species and a new combination in Ligusticopsis made, so that this genus now includes ten recognized species. The species is easily distinguished from other members of Ligusticopsis by the hispid fruit and linear-lanceolate bracteoles.

Figure 1. 

Plastome map of Peucedanum pubescens.

Taxonomic treatment

Ligusticopsis pubescens (Hand.-Mazz.) J.J.Deng, C.K.Liu & X.J.He, comb. nov.

Figs 2, 3

Basionym

Peucedanum pubescens Hand.-Mazz. (1933: 728).

Type

China. Yunnan centralis: In regionis calide temperatae ad orientem fluminis Dsolin-ho, declivibus siccis inter vicos Mabou schan et Bölu, ad elevationem 1900–2000 m, 9 November 1916, Handel-Mazzetti 13043 (lectotype: WU! (WU0029560); isolectotypes: E (E00002620), W!).

Description

Perennials. Plants 30–70 cm, densely pubescent throughout. Stem solitary, hollow, prominent striated protrusions, branches few, short and stout, base densely clothed with fibrous leaf remains. Basal leaves few; petioles with broadly scarious-margined sheaths; leaf blade triangular-ovate in outline, 8–10 × 8–10 cm, 1–2-pinnate, pinnae sessile or subsessile; ultimate segments obovate, 1–4.5 × 0.8–2 cm, rather thick, both surfaces tomentose, more densely so on abaxial nerves, coarsely serrate or crenate, base cuneate or truncate. Leaves reduced upwards, uppermost very small, 3-lobed or toothed, petioles wholly sheathing. Synflorescence subcorymbosely branched; umbels 2.5–4 cm across; peduncles angled; bracts 6 to 8, pinnate and linear coexist, hispid throughout; rays 10 to 15, subequal, 1–2 cm; bracteoles 5 to 7, linear-lanceolate, longer than flowers; umbellules ca. 10-flowered. Calyx teeth conspicuous, subulate. Petals white, stylopodium conical, styles long, ca. 2 mm. Fruit ovate or obovate to orbicular, ca. 4 × 3 mm, hispid; strong dorsal compression, vittae large, 2–3 in each furrow, 6 on commissure. Seed face plane.

Figure 2. 

Peucedanum pubescens A isolectotype (E00002620) B lectotype (WU0029560).

Figure 3. 

Peucedanum pubescens A habit B root C basal leaf D middle leaf E middle leaf with scarious-margined sheaths F bracts and bracteoles G dorsal view of mericarp H transverse section of mericarp. Scale bars: 0.5 mm (G, H).

Phenology

Flowering and fruiting: August to October.

Vernacular name

Máo qián hú (Chinese pronunciation), 毛前胡 (Chinese name).

Distribution and habitat

This species is endemic to China and distributed in Yunnan (Lufeng, Luquan, Wuding) and Sichuan (Huili, Miyi) provinces. It grows in alpine meadows, elevation 1900–3000 m.

Diagnosis

Ligusticopsis pubescens significantly differs from other Ligusticopsis species by linear-lanceolate bracteoles and hispid fruit.

Additional specimen examined

China. Sichuan: Huili, Hongge, 2200 m, 12 October 1958, Z. He, S.G. Tang & B.Q. Li 11593 (NAS); Panzhihua, Baishapo, 26°35'17"N, 101°59'1"E, 1854 m, 17 August 2021, C.K. Liu LCK2020817001 (SZ).

1 Fruit hispid L. pubescens
Fruit smooth 2
2 Bracteoles pinnate and linear coexist 3
Bracteoles pinnate 4
3 Blade shape broadly ovate; calyx teeth linear L. wallichiana
Blade shape triangular-ovate; calyx teeth lanceolate L. brachyloba
4 Bracts pinnate and linear coexist; petals white obcordate L. integrifolia
Bracts pinnate; petals white purplish obcordate 5
5 Commissural vittae 8 L. modesta
Commissural vittae 4 to 6 or 6 6
6 Plants hispid throughout 7
Plants sparsely pilose or glabrous 8
7 Rays extremely elongated, elongate up to 24 cm; calyx teeth linear L. hispida
Rays subequal, (1–)3 cm; calyx teeth lanceolate L. capillacea
8 Stem unbranched; vittae per furrow 1 to 4, commissural vittae 4 to 6 L. scapiformis
Stem usually branched; vittae per furrow1 to 3, commissural vittae 6 9
9 Ultimate leaf segments oblong-ovate; mericarp elliptic L. involucrata
Ultimate leaf segments ovate; mericarp elliptic to ovate L. rechingeriana
Figure 4. 

Phylogenetic tree inferred from Maximum-Likelihood (ML) and Bayesian Inference (BI) analyses based on 79 commonly shared CDs. PP/BS indicated posterior probabilities/bootstrap values.

Figure 5. 

Phylogenetic tree of Peucedanum pubescens inferred from Maximum-Likelihood (ML) and Bayesian Inference (BI) analyses based on 36 ITS sequences. PP/BS indicated posterior probabilities/bootstrap values, respectively. Short line indicates values < 50%.

Acknowledgements

We are grateful to Ziyoviddin Yusupov for his assistance in revising the English. This work was financially supported by the National Natural Science Foundation of China (Grant No. 32170209, 32070221, 31872647), National Herbarium of China, National Herbarium resources teaching specimen database (Grant No. 2020BBFK01).

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