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Research Article
Hansenia trifoliolata, a new species (Apiaceae) from Shaanxi, China
expand article infoQiu-Ping Jiang, Megan Price, Xiang-Yi Zhang, Xing-Jin He
‡ Sichuan University, Chengdu, China
Open Access

Abstract

Hansenia trifoliolata Q.P.Jiang & X.J.He (Apiaceae), is described as new from Shaanxi Province, northwest China. The mericarp features of H. trifoliolata resemble H. himalayensis and H. phaea and molecular phylogenetic analyses (combining ITS and plastid genomes data) suggest that H. trifoliolata is closely related to the group formed by H. oviformis and H. forbesii. The new species H. trifoliolata has unique 3-foliolate leaves and differ from other Hansenia species in its leaves, umbel numbers and size. A comprehensive description of H. trifoliolata is provided, including habitat environment and detailed morphological traits.

Keywords

Apiaceae, Hansenia, new species, phylogenetic analyses

Introduction

The Apiaceae is a large family with high morphological diversity, the generic and tribal delimitations within it being notoriously difficult (Shan and Sheh 1992; Plunkett and Downie 1999). Fruit characteristics have long been regarded as one of the most important sources of evidence for generic and tribal delimitation within the family (Drude 1898; Liu et al. 2003, 2007, 2009; Winter et al. 2008; Magee et al. 2010, 2011).

Notopterygium H. Boissieu (Apiaceae) was first established by Boissieu in 1903 with two species, N. forbesii H. Boissieu and N. franchetii H. Boissieu, which later appeared to be identical (Boissieu 1903). In some later studies, the genus Notopterygium contained six species: N. forbesii, N. forrestii H. Wolff, N. oviforme Shan, N. incisum Ting ex H. T. Chang, N. pinnatiivolucellatum Pu et Y. P. Wang and N. tenuifolium Sheh et Pu (Wolff 1930; Shan 1943; Chang 1975; Pu and Wang 1994; She and Pu 1997; Pu et al. 2000; She and Watson 2005a). The roots of N. incisum and N. forbesii are used in traditional Chinese medicine and named “Qiang Huo” (Wang et al. 1996; She and Watson 2005a; Wei et al. 2019). Although Notopterygium has long been treated as an endemic genus in China, Pimenov et al. (2008) merged it into the genus Hansenia.

Hansenia Turcz. belongs to the East Asia Clade of Apiaceae and it was first established by Turczaninow in 1844, with H. mongolica Turcz. as the type species (Turczaninow 1844; She and Watson 2005a; Pimenov et al. 2008; Downie et al. 2010; Pimenov 2017; Gou et al. 2020). Hansenia used to be treated as a monotypic genus and then some species had been transferred into this genus. Pimenov et al. (2008) transferred all the species of Notopterygium, except N. tenuifolium, to Hansenia through comparative morphological and molecular phylogenetic analyses and proposed five new combinations: H. forbesii (H. Boissieu) Pimenov & Kljuykov, H. forrestii (H. Wolff) Pimenov & Kljuykov, H. oviformis (R. H. Shan) Pimenov & Kljuykov, H. weberbaueriana (Fedde ex H. Wolff) Pimenov & Kljuykov and H. pinnatiinvolucellata (F. T. Pu & Y. P. Wang) Pimenov & Kljuykov (Pimenov et al. 2008; Pimenov 2017). Due to the lack of relevant material, N. tenuifolium was still retained in the genus Notopterygium. Subsequently, based on morphological and molecular data, Jia et al. (2019) considered that H. pinnatiinvolucellata was a synonym of H. weberbaueriana. Additionally, Tan et al. (2020), based on morphological characters and molecular data, transferred the two species of the genus Haplosphaera Handel-Mazzetti (Apiaceae) (She and Watson 2005b) into the genus Hansenia and proposed two new combinations: H. himalayensis (Ludlow) J.B. Tan & X.G. Ma and H. phaea (Handel-Mazzetti) J.B. Tan & X.G. Ma (Tan et al. 2020). Therefore, there are six species in Hansenia and one species in Notopterygium to date.

During a botanical expedition to Feng County in western Shaanxi Province in 2019, a umbelliferous species with thin stem and unusual 3-foliate leaves was collected. Species with 3-foliolate leaves are rare in Apioideae and only Trachydium trifoliatum H. Wolff is known in China (Shan and Sheh 1992). 3-foliolate leaves are commonly found in the genus Sanicula L. (Apiaceae) (She and Phillippe 2005), but the fruits were significantly different from Sanicula. After consulting relevant floras and literature, we identified that the fruit of the new species resembles H. himalayensis and H. phaea and further molecular phylogenetic analyses supported our conclusion. Based on careful morphological and molecular analyses, we identified it as a new species of Hansenia.

Materials and methods

DNA extraction and sequencing

Fresh leaves of Hansenia trifoliolata were collected from wild plants, desiccated and stored in silica gel. The herbarium specimens were stored in the Herbarium, College of Life Sciences, Sichuan University (SZ). Specimen voucher details were provided in Table 1 and Suppl. material 1: Fig. S2. Total genomic DNA was extracted from the stored dry leaves, using a CWBIO plant genomic DNA extraction kit (CWBIO, Beijing, China), following the manufacturer’s protocols. PCR-amplification of the complete ITS region used the primers of ITS4 (5’-TCC TCCGCT TAT TGA TAT GC- 3’) and ITS5 (5’-GGA AGTAAA AGT CGT AAC AAG G-3’; White et al. 1990). PCR amplification was undertaken in a 30 μl volume reaction, containing 3 μl plant total DNA, 1.5 μl of each forward primer and reverse primer, 10 μl ddH2O and 15 μl 2×Taq MasterMix (CWBIO, Beijing, China). The PCR amplification of the nrITS region had an initial denaturation for 4 min at 94 °C, followed by 30 cycles of 45 s at 94 °C, 45 s at 53 °C and 60 s at 72 °C, then a final extension of 10 min at 72 °C. All PCR products were sent to Sangon (Shanghai, China) for sequencing after being examined using a 1.5% (w/v) agarose TAE gel. The DNA sequences of nrITS were applied for phylogenetic analyses and detailed information as outlined in Table 1.

Table 1.

Voucher details and GenBank accession number of Hansenia trifoliolata.

Taxa (Species number) Voucher Locality Genbank number
Plastid genome ITS
Hansenia trifoliolata JQP19082004 Feng County, Shannxi Province OM281945 OM800961
OM800962

Plastid genome sequencing, assembly and annotation

We sequenced, assembled and annotated the plastid genome of Hansenia trifoliolata, then compared it with other species of Hansenia. The processes of plastid genome sequencing, assembly and annotation were performed as follows.

The Illumina Novaseq 6000 platform (Illumina, San Diego, CA, USA) at Novogene (Beijing, China) was used to sequence the resultant DNA with Novaseq 150 sequencing strategy. The remaining clean data were assembled using NOVOPlasty 2.7.1 (Dierckxsens et al. 2017) with the default K-mer value 39 and rbcL of H. oviformis (GenBank accession No.: MF787597.1) being used as seed input. Preliminary genome annotation was conducted using PGA (Qu et al. 2019), with manual modifications for uncertain genes and uncertain start and stop codons, based on comparison with other related plastid genomes, using Geneious R11 soft (Kearse et al. 2012). Protein-coding sequence (CDS) was extracted from the plastid genome using the PhyloSuite programme (Zhang et al. 2020). The plastid genome of H. trifoliolata was submitted to GenBank and the accession number was listed in Table 1.

Phylogenetic analyses

We used MEGA7 (Kumar et al. 2016) to align DNA sequences with manual adjustment to improve the accuracy of sequence alignment. Phylogenetic analyses were undertaken applying Maximum Likelihood (ML) and Bayesian Inference (BI) analyses. Based on the Akaike Information Criterion (AIC) implemented in MrModelTest version 2.2 (Nylander 2004), the best-fit nucleotide substitution models for the ITS sequences (GTR+G) and protein-coding sequences (GTR+G+I) were determined, respectively. ML analyses were undertaken using RAxML v.8.2.4 (Stamatakis 2014) with the best-fit model and 1000 bootstrap replicates. BI analyses were conducted with MrBayes version 3.2 (Ronquist et al. 2012). Four simultaneous runs were performed using Markov Chain Monte Carlo (MCMC) simulations for 10 million generations, starting from a random tree and sampling one tree every 1000 generations. The first 20% of obtained trees were discarded as burn-in and the remaining were used to calculate a majority-rule consensus topology and posterior probability (PP) values.

Results

Morphological study

We collected several specimens of H. trifoliolata from Feng County, Shannxi Province and the type locality at an elevation of 2300–2500 m (Fig. 1). After field observation, we investigated the fruit morphological characteristics of H. trifoliolata (Fig. 2), including fruit shape and size, ribs, vittae and endosperm which are highly similar to H. himalayensis and H. phaea. We compared the morphological characteristics of H. trifoliolata with the related species (H. himalayensis, H. phaea, H. oviformis, H. forbesii and H. forrestii), including life form, leaves, umbel rays and fruits (Table 2).

Table 2.

Diagnostic morphological characters of Hansenia trifoliolata and related species.

Character Taxon
H. trifoliolata H. himalayensis H. phaea H. oviformis H. forbesii H. forrestii
Live form monocarpic polycarpic polycarpic monocarpic polycarpic monocarpic
Plant height (cm) 60–90 80–120 55–90 40–60 80–180 50–100
Leaf in outline (basal) blade broad-triangular, 3-foliolate blade ovate-triangular, 3-pinnate blade broad-triangular or triangular-ovate, ternate-1–2-pinnate broadly triangular 2-pinnate oviform 3-pinnate broadly triangular, 2-pinnate
Median leaflets (pinnae) (basal) cuneate-obovate or rhombic, base cuneate, with irregularly doubly serrate, apex obtuse pinnatifid, pinnae 3–6 pairs, triangular or narrowly ovate-triangular, ultimate segments, mucronate, acute-dentate ovate or obovate, 3-parted, base cuneate; with irregularly doubly serrate or serrate, apex obtuse (broadly) obovate to almost round, base cuneate, margins serrulate, apex obtuse broadly lanceolate to oviform-lanceolate, base obtuse or cuneate, margins serrate oviform to lanceolate, base cuneate, margins irregular or sharply serrate
Lateral leaflets (pinnae) (basal) oblique-ovate, base oblique, often shallowly or deeply uneven 2-parted or not divided; irregularly doubly serrate, apex obtuse pinnatifid, pinnules 3–4 pairs, ultimate segments mucronate, acute-dentate ovate to ovate-lanceolate, base oblique; with irregularly doubly serrate or serrate, apex obtuse ovate or elliptic, base truncate; margins serrulate, apex obtuse broadly lanceolate to oviform-lanceolate, base obtuse or cuneate; margins serrate oviform to lanceolate, base cuneate, base oblique; margins irregular or sharply serrate
Umbels compound umbel, 3–7-rayed, unequal compound umbel, 2–6-rayed, subglobose, unequal Subglobose compound umbel, 5–9-rayed, rays very unequal compound umbel, 11–20-rayed, rays ± equal compound umbel, 6–9-rayed, unequal
Calyx teeth ovate-triangular, 0.3–0.5 mm inconspicuous, triangular, ca. 0.1 mm ovate-triangular, 0.4 × 0.5 mm short, triangular, ca. 0.4 mm short, lanceolate, ca.0.5 mm ovate-lanceolate, 0.3–0.6 mm
Fruit obovoid-oblong or long-ellipsoid, 4–6 mm × 1.4–2.1 mm; constricted at the commissure obovoid-oblong or long-ellipsoid, 6–7 mm × 1.5–2 mm, slightly constricted at the commissure obovoid-oblong, 4–5 mm × 2–2.5 mm; no constricted at the commissure globose, 4–5 × 2–3 mm; no constricted at the commissure oblong-ellipsoid, ca. 5 × 4 mm; no constricted at the commissure subglobose, ca. 3–3.5 × 2.5–3 mm; no constricted at the commissure
Stylopodium conic low-conic depressed flat conic depressed
Mericarp ribs ± equal, prominent to narrow-winged ± equal, conspicuous, narrowly winged ± equal, narrow-winged ± equal, broadly winged ± equal, winged ± equal, winged
Endosperm (at commissural side) concave deeply concave concave slightly concave broadly and not deeply concave concave
Vittae in dorsal furrows 3 (4) 3 3 1–2 2–4 3
Vittae in commissure 2–5 6 4–6 4 4–5 4–6
Figure 1. 

Hansenia trifoliolata in the field A, B habitat C cauline leaves D basal leaves E, F umbels and fruits.

Figure 2. 

Fruit characters of Hansenia trifoliolata A commissural side of fruit B dorsal view of fruit C cross-section of fruit D the illustration of the fruit in transverse section. Voucher: JQP21092801.

Phylogenetic analyses

The phylogenetic analysis result, based on ITS data, is shown in Fig. 3. The details of the ITS dataset that we sequenced for phylogenetic analysis are listed in Table 1. The phylogenetic trees derived from BI and ML analyses were topologically consistent. Thus, only the BI tree is shown in Fig. 3, with bootstrap support values obtained from ML analyses. The phylogenetic tree showed that H. trifoliolata was sister to H. oviformis, with strong support (Bayesian inference posterior probability, BI = 1.00; maximum parsimony bootstrap, ML = 96%). Additionally, H. trifoliolata and other Hansenia species formed a monophyletic group with the support very close to maximum (BI = 1.00; ML = 99%).

Figure 3. 

Bayesian 50% majority-rule consensus tree of Hansenia trifoliolata, other species of Hansenia and related species inferred from ITS sequences using a GTR+G nucleotide substitution model. The tree is rooted with two species of Chamaesium. Maximum Likelihood bootstrap support (ML BS) and Bayesian posterior probabilities (BI PP) are presented at the nodes, * representing the best support (100%). The ITS sequences obtained from NCBI exhibited the GenBank number adjacent to the species names.

The result of the phylogenetic analysis, based on the plastid genome data, is shown in Fig. 4. The plastid genome GenBank number of H. trifoliolata is listed in Table 1. The phylogenetic trees derived from BI and ML analyses were topologically consistent. Therefore, only the BI tree is shown in Fig. 4, with bootstrap support values obtained from ML analyses. The phylogenetic tree showed that H. trifoliolata clustered with the communities of H. oviformis and H. forbesii (BI = 1.00; ML = 68%). This is the same as the ITS tree, with H. trifoliolata and other Hansenia species forming a monophyletic group with maximum support (BI = 1.00; ML = 100%).

Figure 4. 

Bayesian 50% majority-rule consensus tree of Hansenia trifoliolata, other species of Hansenia and related species inferred from protein-coding genes of plastid genomes using a GTR+G+I nucleotide substitution model. The tree is rooted with two species of Chamaesium. Maximum Likelihood bootstrap support (ML BS) and Bayesian posterior probabilities (BI PP) are presented at the nodes,* representing the best support (100%). The plastid genome sequences obtained from NCBI exhibited the GenBank number adjacent to the species names.

Discussion

The fruits of H. trifoliolata were similar to H. himalayensis and H. phaea in fruit shape and size, mericarp ribs and both vittae in dorsal furrows and in the commissure. Additionally, the endosperm (at the commissural side), slightly or deeply concave, was common in Hansenia (Pimenov et al. 2008; Tan et al. 2020). The fruit shape of Hansenia can be divided into two groups by the shape and ribs: fruits oblong-ellipsoid, subglobose or globose, all ribs winged or broadly winged ribs (including H. forrestii, H. forbesii, H. mongolica, H. oviformis and H. weberbaueriana); fruits obovoid-oblong or long-ellipsoid, ribs prominent to narrowly winged (including H. trifoliolata, H. himalayensis and H. phaea). All species’ fruit ribs are 5 and ± equal, except for H. weberbaueriana where the ribs are 3–5, equal or a little unequal (Jia et al. 2019). Moreover, there is a constriction at the commissure in H. trifoliolata, with a similar phenomenon being found in H. himalayensis that has a slight constriction at the commissure (She and Watson 2005a; Tan et al. 2020).

The life form of H. trifoliolata is monocarpic, which is uncommon in Hansenia, except for H. forrestii which seems to be similar (Pimenov et al. 2008). Through observation of the specimens of H. oviformis, we believed that H. oviformis is monocarpic. The leaves of Hansenia species are often 1–3-pinnate, leaflets pinnatifid (including H. mongolica, H. himalayensis and H. weberbaueriana) or leaflets not pinnatifid (including H. forrestii, H. forbesii, H. oviformis, H. phaea and H. trifoliolata). The stylopodium shape in the genus is continuous, from depressed to flat, to low-conic and conic. All species of Hansenia display compound umbels, except for H. phaea and the number of rays are either below ten (including H. trifoliolata, H. himalayensis, H. oviformis and H. forrestii) or ten to twenty (including H. forbesii, H. mongolica and H. weberbaueriana) (Pimenov et al. 2008; Tan et al. 2020).

In our phylogenetic analyses, H. trifoliolata and other Hansenia species formed a monophyletic group in both ITS and plastid trees with very strong support (ITS trees: BI = 1.00, ML = 99%; plastid trees: BI = 1.00, ML = 100%). Though the position of H. trifoliolata within Hansenia had a slight difference between ITS trees and plastid trees (ITS trees: H. trifoliolata was sister to H. oviformis, then clusters with H. forbesii; plastid trees: H. trifoliolata clustered with the communities of H. oviformis and H. forbesii), there is no doubt that H. trifoliolata is a member of the genus Hansenia.

H. trifoliolata overlaps in its distribution with H. forbesii and H. weberbaueriana in the western Shaanxi Province and south-eastern Gansu Province.

The molecular data and morphological evidence strongly support the circumscription of H. trifoliolata as a new species belonging to Hansenia.

Key to the species of Hansenia

1a Fruit oblong-ellipsoid, subglobose or globose or elliptic, all ribs winged or broadly winged, wings equal or unequal 2
2a Rays below ten, unequal 3
3a Ultimate leaf segments ovate-lanceolate, 2.5–8 cm; bracteoles linear, shorter than flowers H. forrestii
3b Ultimate leaf segments ovate, 1.5–3.5 cm; bracteoles filiform, longer than flowers H. oviformis
2b Rays ten to twenty, ± equal 4
4a Leaves pinnatisect, leaflets pinnatifid 5
5a Bracteoles linear or pinnatifid, fruit ribs 3–5, ultimate leaf segments oblong, margin pinnatifid or variously laciniate-dentate H. weberbaueriana
5b Bracteoles linear, ribs 5, ultimate leaf segments broadly ovate to oblong, at the margin toothed, teeth obtuse H. mongolica
4b Leaves pinnate, leaflets not pinnatifid, ultimate leaf segments ovate to oblong-ovate, margin entire or coarsely toothed H. forbesii
1b Fruit obovoid-oblong or long-ellipsoid, ribs prominent to narrowly winged 6
6a Basal leaves and cauline leaves 3-foliolate, umbels 2–5 cm across, rays unequal H. trifoliolata
6b Basal leaves ternate-1–3-pinnate, flowers densely crowded into a compact, globose heads 7
7a Basal leaves ternate-1–2-pinnate; petals obovate, apex narrowly inflexed H. phaea
7b Basal leaves 3-pinnate; petals broad-ovate, spoon-shaped apex acute H. himalayensis

Description of the new species

Hansenia trifoliolata Q.P.Jiang & X.J.He, sp. nov.

Figs 1, 5; Suppl. material 1: Fig. S2

Diagnostic characters

Monocarpic. Root cylindrical, branched or partial rhizomes. Leaves 3-foliolate. Umbels 2–5 cm across, rays 3–7, unequal. Stylopodium conical. Fruits are obovoid-oblong or long-ellipsoid, have 5 ribs, ribs prominent to narrow-winged and endosperm (at commissural side) concave. It is clearly distinguished from H. phaea and H. himalayensis in leaves (ternate-1–2-pinnate and 3-pinnate vs. 3-foliolate). Compared to other Hansenia species (i.e. H. forrestii, H. oviformis and H. forbesii), H. trifoliolata also shows distinctive morphological characters, especially in fruits characters (shape and ribs) and leaves (3-foliolate is unique in Hansenia).

Figure 5. 

Holotype of Hansenia trifoliolata, fruiting. Vouchers: JQP21092801.

Type

China, Shaanxi Province: Tongtianhe National Forest Park, Feng County, elevation 2430 m a.s.l., 34°14'N, 106°33'E, 28 Sep 2021, Q. P. Jiang, JQP21092801, fruiting (Holotype: SZ).

Description

Biennial, herb, 60–90 cm high. Root cylindrical, branched or partial rhizomes. Stem purplish-green, thinly ribbed, glabrous, thin. Leaves 3-foliolate, green, blade broad-triangular, irregularly doubly serrate, teeth mucronate; central leaflets cuneate-obovate or rhombic, 4–6 × 2–3.5 cm, with irregularly doubly serrate, base cuneate; lateral leaflets oblique-ovate, base oblique, often shallowly or deeply uneven 2-parted or not divided, 2–5 × 3.5–6.5 cm. Basal petioles 15–20 cm, petioles shorten upwards; sheaths narrow-oblong, glabrous, with margin irregularly coarse-cuspidate-serrate. Umbels 20–50 mm across; peduncles 5–20 mm long, glabrous; bracts 0 to 2, linear; rays 3 to 7, 5–25 mm long, glabrous; bracteoles 2 to 7, linear, 3–8 mm long; raylets 5 to 11, 1–3 mm long. Flowers unknown; calyx teeth ovate-triangular, 0.3–0.5 mm; petals unknown; stylopodium conical. Fruit obovoid-oblong or long-ellipsoid, 1.4–2.1 × 4–6 mm; mericarps 5-ribbed, ribs prominent to narrow-winged; vittae 3 (4) in each furrow, 2–5 on commissure; endosperm (at commissural side) concave, commissure width 0.8–1.35 mm.

Etymology

The specific epithet refers to the distinctive 3-foliolate leaves.

Phenology

Flowering from July to August, and fruiting from August to September.

Distribution, habitat and ecology

At present, this new species has only been found in the type locality in Tongtianhe National Forest Park, Feng County, Shaanxi Province, China. According to the growing environment, we speculate it may inhabit forests at an elevation of 2300 m to 2500 m in western Shaanxi Province and south-eastern Gansu Province. This new species grows in humid environments under the forests.

Additional specimens examined

(paratypes). China: Shaanxi Province, Baoji City, Feng County, Tongtianhe National Forest Park, elevation 2430 m a.s.l., 34°14'N, 106°33'E, 20 Aug 2019, Q. P. Jiang and X. Y. Zhang, JQP19082004 (photo SZ !).

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 32070221, 32170209, 31872647), National Herbarium of China, National Herbarium resources teaching specimen database (Grant No. 2020BBFK01).

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Supplementary material

Supplementary material 1 

Figure S1, S2

Qiu-Ping Jiang, Megan Price, Xiang-Yi Zhang, Xing-Jin He

Data type: Docx file.

Explanation note: Figure S1. Fruit of Hansenia trifoliolata. Figure S2. Isotype of Hansenia trifoliolata and paratype of H. trifoliolata.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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