Research Article |
Corresponding author: Quan-Ru Liu ( liuquanru@bnu.edu.cn ) Academic editor: Alexander Sennikov
© 2024 Li-Hua Wang, Xue-Min Xu, Yi He, Quan-Ru Liu.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wang L-H, Xu X-M, He Y, Liu Q-R (2024) The identity of Bupleurum jeholense (Apiaceae). PhytoKeys 237: 231-243. https://doi.org/10.3897/phytokeys.237.111977
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Bupleurum jeholense Nakai (Apioideae, Apiaceae), originally found in the Wuling Mountain of China, was initially described as a species but later treated as a variety of B. sibiricum Vest ex Spreng. However, researchers have recently found that it is more closely related to B. chinense DC. In this study, we conducted morphological and phylogenetic analyses as well as chromosome counting to determine the taxonomic status of B. sibiricum var. jeholense (Nakai) Chu. Our results showed that B. sibiricum var. jeholense and B. chinense share common features (i.e., bracteoles 5 and stem solid) that distinguish both from B. sibiricum var. sibiricum. The chromosome number of B. sibiricum var. jeholense was found to be the same as in B. chinense (i.e., 2n = 12), whereas the chromosome number of B. sibiricum var. sibiricum was 64. A phylogenetic tree based on complete chloroplast genome data revealed a close relationship between B. sibiricum var. jeholense and B. chinense. Finally, B. sibiricum var. jeholense and B. chinense were mainly found to differ in plant height, number of stems, and middle stem leaves. Based on this evidence, we propose a new combination: Bupleurum chinense var. jeholense (Nakai) Q.R.Liu & L.H.Wang.
Apiaceae, Bupleurum chinense DC. var. jeholense (Nakai) Q.R.Liu & L.H.Wang, new combination
Bupleurum is a monophyletic genus in the tribe Bupleureae (Apioideae, Apiaceae) (
Bupleurum jeholense Nakai was initially described on the basis of specimens collected from the Wuling Mountain (China). Nakai stated that the characters of this species are as follows: middle stem leaves oblanceolate, base tapering, apex obtuse or acute, apiculate, bracteoles 5, exceeding flowers (
During recent fieldwork on Dongling Mountain (Beijing, China), we found that the distribution of Bupleurum species was closely linked to altitude. Normally, B. chinense is distributed at low altitudes (<1600 m). However, with the increasing altitude, we found a continuous variation in B. chinense; for example, plants became shorter; the number of branches decreased; the number of bracteoles gradually changed from 3 to 5 and varied in length from obviously shorter than the umbel to almost equal. Furthermore, as the altitude increased to 1600 m, B. chinense was gradually replaced by B. sibiricum var. jeholense. After checking the specimens, we also found that there were misidentifications between B. chinense and B. sibiricum var. jeholense. Subsequent phylogenetic analyses of Chinese Bupleurum spp. based on nrDNA ITS and chloroplast markers (i.e., trnH-psbA and matK) indicated that B. sibiricum var. jeholense was more closely related to B. chinense, whereas B. sibiricum var. sibiricum was closely related to B. smithii Wolff (
We therefore collected and checked several specimens from the type locality of B. jeholense. We conducted morphological observations, statistical comparisons, cytological studies, and a phylogenetic analysis based on the complete chloroplast genome to clarify the relationship among B. sibiricum var. jeholense, B. sibiricum var. sibiricum, and B. chinense.
Using the existing scientific literature and the relevant type specimens, we collected new specimens from the type locality of B. sibiricum var. jeholense and compared these with images of the type specimens. Specimens from field collections, CVH (https://www.cvh.ac.cn/), and online herbarium collections (MW, LE) were used to count bracteoles. In total, we obtained bracteole count data for 129 specimens of B. sibiricum var. jeholense, 183 specimens of B. sibiricum var. sibiricum, and 183 specimens of B. chinense. We analyzed these data using R (beanplot package) to produce boxplots (
All materials used for cytological studies were obtained from the Wuling Mountain (B. sibiricum var. jeholense), Wutai Mountain (B. chinense), and Daqing Mountain (B. sibiricum var. sibiricum). All voucher specimens are listed in Table
Voucher information and GenBank accession numbers for newly sequenced plastome sequences.
Taxon | Location | Voucher information | Accession |
---|---|---|---|
B. chinense | Dongling Mountain, Beijing, China | BNU2021HB002 (BNU) | OR387523 |
B. smithii | Xiaowutai Mountain, Hebei, China | BNU2020DT007(BNU) | OR387522 |
B. sibiricum var. sibiricum | Daqing Mountain, Inner Mongolia, China | BNU2021NMG017(BNU) | OR387525 |
B. sibiricum var. jeholense | Wuling Mountain, Hebei, China | BNU2021HB025(BNU) | OR387524 |
Fresh plant leaves were collected from the field and quickly dried with silica gel for DNA extraction. Specimen voucher information is shown in Table
In total, 25 sequences were imported into PhyloSuite (
The bean plot indicated that the number of bracteoles of B. sibiricum var. jeholense was mostly 5 and occasionally 6, whereas that of B. sibiricum var. sibiricum was (6)7–8(9). Bupleurum chinense had 5, sometimes 4 or even 3 bracteoles at lower elevations or in an understory (Figs
Comparison of the morphological characteristics and geographic distributions of three taxa under study.
Character | B. chinense | B. sibiricum var. jeholense | B. sibiricum var. sibiricum |
---|---|---|---|
Height | 40–90 cm | 20–40 cm | 30–70 cm |
Stem (number) | Single, occasionally several | Many, clustered | Many, clustered |
Stem (branching) | 2–4-branched | 1–2-branched | 1–2-branched |
Stem (presence of cavity) | Solid | Solid | Hollow in all internodes |
Basal leaves | Withering early | Withering early | Persistent, many |
Basal leaf size | 4–7 × 0.6–0.8 cm | 5–10 × 0.3–0.8 cm | 12–25 × 0.7–1.6 cm |
Middle stem leaves | 4–12 × 0.6–1.8 cm | 6–12 × 0.5–1.2 cm | 6–14 × 0.5–1.6 cm |
Middle stem leaf length to width ratio | 6–10 | 10–16 | 10–14 |
Upper stem leaves | Not embracing | Not embracing | Rounded-cuneate, embracing |
Bracteole relative length | Shorter than flowers | Shorter than or equal to flowers | Exceeding flowers |
Bracteoles | (3–4) 5, lanceolate | 5 (6–7), lanceolate | (6) 7–12, elliptic-lanceolate |
Distribution | Northeast and Central China | Yan mountains (Hebei and Beijing) | Heilongjiang, Liaoning, Inner Mongolia, Mongolia, and Russia |
Cytological analysis revealed that the chromosome number of B. sibiricum var. jeholense was 2n = 12 (x = 6), i.e., the same as B. chinense but different from B. sibiricum var. sibiricum (2n = 64, x = 8) (Fig.
The size of the four Bupleurum chloroplast genomes ranged from 155,706 to 155,858 bp. The complete chloroplast genome had a typical circular quadripartite structure and consisted of a pair of inverted repeat regions separated by the large single copy and small single copy regions. The topologies of the ML and BI trees constructed using the cp genome sequences were consistent. These results showed that the genus Bupleurum can be divided into two clades, with all Chinese Bupleurum plants belonging to B. subg. Bupleurum. Bupleurum sibiricum var. sibiricum was found to cluster with B. smithii and B. bicaule Helm (BS = 100% PP = 1), whereas B. chinense was found to cluster with B. sibiricum var. jeholense (BS = 100% PP = 1) and was more distantly related to B. longiradiatum Turcz., B. falcatum L. and B. boissieuanum H. Wolff (Fig.
Botanists have closely monitored the number of bracteoles because this character is essential in the taxonomy of Bupleurum. Moreover, bracteole number is an important indicator of the taxonomic position of B. sibiricum var. jeholense in the genus. Five bracteoles are generally present in both B. chinense and B. sibiricum var. jeholense. However, in environments such as the understory, B. chinense may have only three or four bracteoles. Furthermore, 6–7 bracteoles have occasionally been observed in B. sibiricum var. jeholense. We observed that the number of bracteoles in B. sibiricum samples collected from the Daqing Mountain, which were collected at the same latitude and altitude as the samples collected from Wuling Mountain, was not 5, as would be expected for B. sibiricum var. jeholense. Thus, we speculated that the 5-bracteoled B. sibiricum var. jeholense may not have evolved from the 12-bracteoled B. sibiricum var. sibiricum.
In the classification of the genus Bupleurum, stem structural characteristics have rarely been examined. After observing numerous specimens, we found that the stem of B. sibiricum var. sibiricum was hollow and contained a substantial cavity. In contrast, the stems of B. chinense and B. sibiricum var. jeholense lacked this cavity. The presence or absence of a stem cavity is a stable character and does not change with the period of growth. For example, B. komarovianum was once treated as a variety of B. chinense (
Bupleurum chinense is widely distributed throughout East Asia and is often cultivated as a medicinal plant. The morphology of this species varies with the environment. Bupleurum sibiricum var. jeholense may be a variant of B. chinense that has adapted to the cold environments found in high-altitude mountains. In particular, the bracteole number may have increased to protect flowers at higher altitudes (
Chromosomal variation plays a vital role in species formation, and the diversity of chromosome size and number is therefore an important character that can be used to track Bupleurum species that have adapted to different habitats (
In this study, a phylogenetic tree was reconstructed using chloroplast genome data. Our findings were consistent with those of
Bupleurum sibiricum is distributed widely throughout temperate Asia. It often co-occurs with B. scorzonerifolium in arid meadows in Inner Mongolia and Siberia at elevations of 700–2000 m. In the field, B. sibiricum var. jeholense is often found to co-occur with B. chinense at different altitudes in the same mountain. At present, B. sibiricum var. jeholense is found only in high-altitude areas of the Yan Mountains. Moreover, it has a narrow distribution area and is confined to altitudes of 1500–2000 m. In contrast, B. chinense is widely distributed and is found at altitudes ranging from 200 to 1600 m in Northeast China; however, it has also been found isolated at an altitude of 2100 m in Northwest China. Given these findings, we speculate that B. sibiricum var. jeholense is a specialized morphological variant of B. chinense that has specifically adapted to high altitudes. Overall, in terms of distribution and habitat, B. sibiricum var. jeholense differs considerably from B. sibiricum and is more similar to B. chinense.
– Bupleurum jeholense Nakai in J. Jap. Bot. 13: 482 (1937) – Bupleurum sibiricum var. jeholense (Nakai) Chu in Shan & Li, Acta Phytotax. Sin. 12 (3): 272 (1974).
= Bupleurum jeholense var. latifolium Nakai in J. Jap. Bot. 13: 482 (1937). Type. China. Hebei: Wuling Mountain, 1800 m, 2 Sept 1933, Nakai, Honda et Kitagawa s. n. (holotype: TI0082957!).
Bupleurum chinense var. jeholense is morphologically similar to var. chinense and can be distinguished from the latter by plant size (>40 cm), the presence of multiple stems, with 1–2 branches per stem, thinner middle stem leaves, leaf length to width ratio 10–16, and the presence of 5 bracteoles.
Plants 20–40 cm, perennial. Root stout, brown, woody. Stem solitary or several, solid, petioles often purplish-red, clasping base without fibrous remnant sheaths. Basal leaves oblanceolate, 5–10 × 0.3–0.8 cm, base petioles, apex acuminate. Middle leaves sessile, oblanceolate, 4.5–12 × 0.4–1.4 cm, 7–9-nerved, base tapering, apex obtuse or acute, apiculate. Apical leaves small. Umbels 5–12, nearly equal or unequal rays 0.4–4 cm long; bracts of 1–5 unequal leaflets, often obsolete or deciduous, 3–15 × 0.6–11 mm, 4–7-nerved; bracteoles 5, lanceolate, 3–7 × 0.6–0.8 mm, exceeding flowers; umbellule 4–12 mm across, 8–14-flowered. Petals bright yellow. Stylopodium low-conic, discoid, dark yellow. Fruit oblong, brown, ca. 2.2–3.5 × 0.9–1.5 mm; ribs prominent, narrowly winged, wings pale brown; vittae 3(–4) in each furrow, 4 on commissure (Fig.
Flowering and fruiting from August to October.
Hebei, Beijing. It grows in mountains at elevations of 1500–2000 m.
China. Beijing: Fangshan county, Jin-Wu Wang s.n. (PEY!); Mentougou county, Xiao-Liu QS-186 (BJFC!); Quan-Ru Liu 200609009 (BNU!); Xue Lin 05 05-4-114 (BJFC!); Gang-Min Zhang 201008036 (BJFC!); Xian-Yun Mu 1821 (BJFC!); Duan-Zheng Lu s.n. (BJFC!); Quan-Ru Liu DL025-2 (BNU!); Quan-Ru Liu DL026-2 (BNU!); Quan-Ru Liu DL027-1 (BNU!); Miyun county, Xian-Yun Mu 1924 (BJFC!). Hebei: Xinglong county, Li-Hua Wang BNU2021HB029 (BNU!); Li-Hua Wang BNU2021HB025 (BNU!); Jia-Yi Liu 0845 2190 (TIE!); Jin-Wu Wang s.n. (PEY!); Zhen-Fu Fang 825 (NAS!); Ze-Hui Pan 83940 (NAS!); Ze-Hui Pan 83939 (NAS!); Shen-E Liu 4833 (IFP!); Zhen-Fu Fang 826 (IFP!); Quan-Ru Liu WLS068 (BNU!); Xin-Yuan Liu 1652 (KUN!); Jia-Yi Liu 08450 (TIE!); Jia-Yi Liu 00485 (TIE!); Biaobenshi 2190 (PE!); Wu-Xiu Zhang 91 (PE!).
We gratefully acknowledge the collaboration of the curators and staff of the herbaria mentioned in the text for their assistance upon visits, as well as for access to digital specimen images. Special thanks are due to Professor Akiko of the University of Tokyo for kindly providing photographs of the type specimens. We thank Dr. Dan-Hui Liu for the analyses of molecular sequence data and Xun Sun for the field assistance.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This research was funded by the Biodiversity survey and assessment project of the Ministry of Ecological Environment (2019HJ2096001006).
Funding acquisition: QRL. Investigation: LHW. Software: XMX, LHW. Supervision: QRL. Writing – review and editing: YH, XMX, LHW.
Yi He https://orcid.org/0000-0002-6925-7299
Quan-Ru Liu https://orcid.org/0000-0003-4270-4746
All of the data that support the findings of this study are available in the main text.