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Research Article
Phylogenetic and taxonomic studies of six recently-described Stellaria species (Caryophyllaceae) from China, with an additional new species, Stellaria longipedicellata, from Sichuan
expand article infoWenqiao Wang‡, Zhiwei Su‡, Zhonghui Ma‡
‡ Guangxi University, Nanning, China

Corresponding author: Zhonghui Ma ( mazhonghui@gxu.edu.cn )

Academic editor: Alexander Sukhorukov
© 2024 Wenqiao Wang, Zhiwei Su, Zhonghui Ma.
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 W, Su Z, Ma Z (2024) Phylogenetic and taxonomic studies of six recently-described Stellaria species (Caryophyllaceae) from China, with an additional new species, Stellaria longipedicellata, from Sichuan. PhytoKeys 249: 287-298. https://doi.org/10.3897/phytokeys.249.136456
Open Access

Abstract

The phylogenetic studies of the tribe Alsineae (Caryophyllaceae) have revealed a clearer boundary between the genus Stellaria and related genera, primarily relying on the morphological characteristics of style 3, stamens 10 and petals deeply bifid. However, the newly-published species in China, which have 5 styles or ten or more lobes per petal, challenge this boundary and necessitate further studies. In this paper, we reviewed six newly-published Chinese species of Stellaria, utilising both molecular phylogenetic evidence from nuclear ribosomal internal transcribed spacer (ITS) and four plastid regions (trnL-F, matK, rbcL, rps16) and morphological evidence. Our results demonstrated that the five new species (Stellaria abaensis, S. multipartita, S. pentastyla, S. procumbens and S. zhuxiensis) were nested within the genus Stellaria, but Stellaria motuoensis was sister to the genus Schizotechium. Herein, we accepted four new Stellaria species and proposed a new combination in Schizotechium and a new synonym in Stellaria. Additionally, we described a new species Stellaria longipedicellata from Sichuan Province, China, which was distinguished from the closely-related species Stellaria decumbens by its glabrous body, linear-lanceolate leaves, long pedicellate flowers, prostrate growth habit and flowers nearly equal to or slightly shorter than sepals. Both molecular and morphological evidence support the treatment of S. longipedicellata as a new species of the genus Stellaria.

Key words

Alsineae, new combination, new species, Stellaria

Introduction

The classification of three subfamilies has been widely accepted in the family Caryophyllaceae (Lu et al. 2001). Since the establishment of phylogenetic tree of Caryophyllaceae, the classification of eleven tribes has been increasingly accepted (Harbaugh et al. 2010; Greenberg and Donoghue 2011). The tribe Alsineae, as a major branch of Caryophyllaceae with a great diversity of species, has attracted much attention. Recent studies on the tribe Alsineae have clarified the boundaries of its genera and have described the following new genera: Engellaria Iamonico, Hartmaniella M.L.Zhang & Rabeler, Nubelaria M.T.Sharples & E.A.Tripp, Rabelera M.T.Sharples & E.A.Tripp, Shivparvatia Pusalkar & D.K.Singh, Hesperostellaria Gang Yao, B. Xue & Z.Q. Song, Reniostellaria Gang Yao, B. Xue & Z.Q. Song and Torreyostellaria Gang Yao, B. Xue & Z.Q. Song (Zhang et al. 2017; Sharples and Tripp 2019; Iamonico 2021; Pusalkar and Singh 2022; Xue et al. 2023). Stellaria L. is particularly noteworthy as one of the genera with a high species richness in the tribe Alsineae, mainly characterised by 4 or 5 petals, petals usually deeply bifid (rarely retuse or multilobed) and capsules opening by valves 2 times number of styles (Chen and Rabeler 2001). Despite the species richness of this genus, limited research has been conducted on it. Previous phylogenetic studies of the family Caryophyllaceae have proposed that the traditional Stellaria was paraphyletic (Harbaugh et al. 2010; Greenberg and Donoghue 2011; Dillenberger and Kadereit 2014; Zhang et al. 2017). Due to the global studies on Stellaria, its classification has been clarified and species with non-deeply-bifid petals or 2 styles have been assigned as the following new genera: Nubelaria, Rabelera, Hesperostellaria, Reniostellaria and Torreyostellaria (Sharples and Tripp 2019; Xue et al. 2023). Then the core Stellaria in a new circumscription can be clearly distinguished from other related genera in having deeply-bifid petals (sometimes absent) usually in combination with six-valved capsules (Sharples and Tripp 2019). However, there is still a lack of research on new species of Stellaria with distinctive petals found in China.

In recent publications, six new Stellaria species have been documented in China, described as Stellaria abaensis H.F. Xu & Z.H. Ma, S. motuoensis Meng Li & Y.F. Song, S. multipartita Bo Xu & Meng Li, S. pentastyla W.Q. Wang, H.F. Xu & Z.H. Ma, S. procumbens Huan C. Wang & Feng Yang and S. zhuxiensis Q.L. Gan & X.W. Li. (Gan and Li 2014; Xu and Ma 2018; Song et al. 2020; Wang et al. 2020; Yang et al. 2020; Li et al. 2022). Amongst them, only three species (S. motuoensis, S. multipartita and S. pentastyla) were supported by the phylogenetic study, while the precise phylogenetic position of the remaining species requires further investigation. Notably, four species exhibit distinct flower morphology compared to the core Stellaria species. For instance, S. motuoensis lacks petals and bears 5 stamens, S. multipartita displays ten or more lobes per petal, while S. pentastyla and S. procumbens have 5 styles. Furthermore, two species share similar morphological characteristics with related species, such as S. abaensis and S. petiolaris Hand.-Mazz., S. zhuxiensis and S. vestita Kurz. Further in-depth research is crucial for a comprehensive understanding of these newly-named Stellaria species.

In addition, during a field survey in Sichuan Province of China, we discovered an undescribed species whose morphology does not correspond to any known Stellaria species. Based on detailed morphological and molecular studies, we hereby describe it as a new species.

Materials and methods

Sample and morphology

In this study, we sampled major genera of the tribe Alsineae and major clades of Stellaria in order to accurately determine the phylogenetic position of the new species, with Arenaria serpyllifolia L. serving as the outgroup. Samples and accession numbers are listed in Table 1, Suppl. material 1. The morphological traits of the new species were examined by either the original specimens or their images and also by specimens collected through our own field surveys.

Table 1.
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Taxa sampled and the vouchers.

Taxon Location Latitude, Longitude Collector and number Herbarium
Stellaria abaensis H.F. Xu & Z.H. Ma Tianquan, Sichuan 31.049472, 102.874177 H.F. Xu SC0037 GAUA
Stellaria amplexicaulis (Hand.-Mazz.) Huan C. Wang & Feng Yang Luding, Sichuan 26.016249, 98.620941 H.F. Xu & G.F. Mou YN0002 GAUA
Stellaria procumbens Huan C. Wang & Feng Yang Luding, Sichuan 29.851945, 102.286631 W.Q. Wang et al. QSC0007 GAUA
Stellaria radians L. Yakeshi, Neimenggu 49.327739, 120.676409 W.Q. Wang & R. Wu NM0010 GAUA
Stellaria longipedicellata W.Q. Wang & Z.H. Ma Luding, Sichuan 29.863690, 102.289755 W.Q. Wang et al. QSC0009 GAUA
Stellaria zhuxiensis Q.L.Gan & X.W.Li Zhuxi, Hubei 32.436378, 109.561435 W.Q. Wang & Z. Xie HB0034 GAUA

Phylogenetic analysis

Total DNA was extracted from silica gel dried leaves by modified CTAB (Doyle and Doyle 1987). Subsequently, we performed PCR amplification of the following markers as cited, ITS (5F, 4R), matK (390F, 1440R), rbcL (1F, 724R), rps16 (F, R) and trnL-F (C, F) (White et al. 1990; Taberlet et al. 1991; Popp and Oxelman 2001; Smissen et al. 2002; Kress and Erickson 2007). The PCR products were then sequenced by the Beijing Genomics Institute (BGI). The obtained sequences were double-stranded spliced and checked using GENEIOUS v.11.0.4 (Kearse et al. 2012) and the phylogenetic trees were conducted using PHYLOSUITE v.1.2.2 (Zhang et al. 2020). Initially, the sequences were aligned by MAFFT v.7.313 (Katoh and Standley 2013). Then we used PARTITIONFINDER v.2.1.1 (Lanfear et al. 2016) to determine the best model under the Akaike Information Criterion (AIC). The selected models were SYM+I+G for ITS, GTR+G for matK, trnL-F, and rps16 and HKY+I+G for rbcL. The Bayesian Inference (BI) trees were constructed using MrBayes 3.2.6 (Ronquist et al. 2012) with 2,000,000 generations and the tree sampled every 100 generations. The first 25% trees of each run were discarded as burn-in. To assess the chain convergence, it was verified that the average standard deviation (SD) of the split frequencies was below 0.01. Finally, Maximum Likelihood (ML) trees were constructed using the GTRGAMMA model with 1,000 bootstrap replicates and default values for the remaining parameters on the CIPRES Science Gateway (Miller et al. 2010). No notable incongruence was found between the nrITS phylogenetic tree and the plastid phylogenetic tree.

Results

In the phylogenetic tree of the tribe Alsineae (Fig. 1), Stellaria formed a single clade, except for Stellaria motuoensis. Our results revealed that five new species (S. abaensis, S. multipartita, S. pentastyla, S. procumbens and S. zhuxiensis) were nested within Stellaria, but S. motuoensis was sister to Schizotechium with high support (BS = 100%, PP = 1.00). Stellaria procumbens was nested within the Larbreae clade and identified as the sister to S. pentastyla (BS = 100%, PP = 1.00). Notably, S. abaensis and S. zhuxiensis fell into the Larbreae clade and were sister to each other. Then S. multipartita was clustered with S. pubera Michx. and S. corei Shinnersin, forming the Insignes clade. Finally, S. longipedicellata, a potential new species was sister to S. decumbens Edgew.

Figure 1. 

Maximum likelihood (ML) tree of Alsineae inferred from the Alsineae-wide dataset (including nrITS, matK, rbcL, rps16 intron and trnL-F intergenic region). Posterior probability (PP) in Bayesian Inference (BI) and bootstrap (BS) value in ML analysis are indicated above and below the stem branch of each phylogenetic node, respectively. NP indicates the topology was not present in BI analysis. * indicates that the PP or BS value is less than 0.5 or 50%.

Discussion

Sect. Schizothecium Fenzl, a traditional section of the genus Stellaria, is characteried by having 3 styles and 1–2 seeds. It includes S. delavayi Franch., S. monosperma Buch.-Ham. ex D. Don and S. ovatifolia (Mizushima) Mizushima (Wu and Ke 1996). However, recent studies proposed that sect. Schizothecium should be resurrected as the genus Schizotechium (Pusalkar and Srivastava 2016; Arabi et al. 2022; Wang et al. 2023; Xue et al. 2023). Consequently, Stellaria delavayi and S. monosperma of sect.Schizothecium were reclassified under the genus Schizotechium (Pusalkar and Srivastava 2016; Xue et al. 2023). Moreover, it has been suggested that S. ovatifolia should revert to its previous name Brachystemma ovatifolium M. Mizush. (Wang et al. 2023). When S. motuoensis was published, it exhibited morphological similarities with S. monosperma var. paniculata (Edgew.) Majumdar and was sister to S. monosperma in the phylogenetic tree (Li et al. 2022). However, authors still considered S. motuoensis as part of Stellaria due to uncertainty of the phylogenetic tree of the tribe Alsineae and its morphological differences with Schizotechium species (Li et al. 2022). Nonetheless, more recent studies on the tribe Alsineae have accepted the genus Schizotechium (Pusalkar and Srivastava 2016; Arabi et al. 2022; Wang et al. 2023; Xue et al. 2023). Our study also indicated that S. motuoensis was nested within Schizotechium and sister to Schizotechium monosperma with high support (BS = 100, PP = 1.00, Fig. 1), which is consistent with previous studies (Li et al. 2022). Importantly, S. motuoensis (with many-flowered compounds cymes, 5 stamens, 2–3 styles and 1–3 seeds; see Table 2) is morphologically more similar to Schizotechium (with many-flowered compounds cymes, 5 stamens, 2–3 styles and 1–3 seeds compound cymes, 5 or 10 stamens, 2–3 styles and 1–6 seeds; see Table 2), rather than the core Stellaria (with lax dichasial cymes, rarely solitary, 10 stamens, 3 or 5 styles and numerous seeds) (Pusalkar and Srivastava 2016; Arabi et al. 2022, Li et al. 2022). Based on the morphological and phylogenetic evidence, we propose a new combination for Stellaria motuoensis.

Table 2.
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Morphological comparisons of six species.

S. motuoensis Schizotechium monosperma S. procumbens S. pentastyla S. longipedicellata S. decumbens
Petal absent 2-lobed to middle deeply bifid deeply bifid deeply bifid deeply bifid
Stem glabrous basally, pubescent in apical part pubescent with 1 or 2 rows of glandular hairs above glabrous glabrous glabrous densely white pubescent
Style 2–4 3 3 or 5 5 3, rarely 4 3
Leaf shortly petiolate, lamina ovate or oblong short or long petiolate, lanceolate or oblong-lanceolate to elliptic sessile, linear or acicular sessile, linear sessile, linear-lanceolate sessile, oblong
Seed 1–3 1–2 numerous numerous numerous numerous
Pedicel pubescent pubescent glabrous glabrous glabrous pubescent
Stamen 5 10 10 10 10 10

Presence of the stellate hair is a highly distinctive character in Stellaria including S. vestita, S. infracta Maximowicz and S. amplexicaulis (Hand.-Mazz.) Huan C.Wang & Feng Yang (Chen and Rabeler 2001; Yang et al. 2020). Stellaria zhuxiensis closely resembles S. vestita with its sessile leaf and dense stellate indumentum, but differs by its longer petals and ovate leaves (Gan and Li 2014). Interestingly, S. zhuxiensis was sister to S. abaensis, not to any other of the stellate-haired species (Fig. 1). Our findings were consistent with the previous studies, which indicated that S. vestita and S. infracta with stellate hairs were not sister taxa on the phylogenetic tree (Sharples and Tripp 2019). It could be attributed to the parallel evolution of stellate trichomes (Sharples 2019).

The classification of ser. Petiolares is widely accepted within Stellaria, characterised by the presence of distantly petiolate leaves (Endlicher 1840; Schischkin 1970; Wu and Ke 1996). The latest Stellaria phylogenetic study also kept the classification of the Petiolares clade (Sharples and Tripp 2019). Stellaria abaensis with long petioles was closely similar to the Petiolares clade species (Xu and Ma 2018). However, it is intriguing to discover that S. abaensis nested in the Larbreae clade instead of being associated with the Petiolares clade (Fig. 1). Similarly, being consistent with the previous studies (Sharples and Tripp 2019), petiolate species such as S. vestita and S. petiolaris were placed in the Larbreae clade rather than the Petiolares clade (Fig. 1). Hence, the presence of petiolate or sessile traits may not be reliable indicators for classification within Stellaria. Additionally, it is worth noting that S. abaensis was often misidentified as S. petiolaris before its official publication. For instance, S. capillipes (Franch.) C. Y. Wu (the synonymy of S. petiolaris) referred numerous specimens of S. abaensis and the description and pictures of S. petiolaris in the Flora of Yunnan actually corresponded to S. abaensis (Wu 1995). However, S. abaensis can be easily distinguished from S. petiolaris due to its glabrous leaves and long petiole with ciliate hair (vs. leaves and short petiole densely covered with white villous hair), glabrous plant body (vs. plant body densely covered with white villous hair), petal lobes ovate-oblong (vs. lobes narrowly linear) and the capsule longer than persistent sepals (vs. capsule ca. 1/2 as long as persistent sepals) (Chen and Rabeler 2001; Xu and Ma 2018).

The traditional Stellaria did not include species with five styles, which is commonly found in the related genus Cerastium L. (Chen and Rabeler 2001). However, since S. aquatica (L.) Scop. (Myosoton aquaticum (L.) Moench) was included within Stellaria, the genus Stellaria recently also includes five-styled species (Sharples and Tripp 2019; Wang et al. 2020; Xu et al. 2020; Yao et al. 2021; Arabi et al. 2022; Xue et al. 2023). This study revealed that S. pentastyla and S. procumbens bearing 5 styles are not sister to the clade including S. aquatica (Petiolares clade), but constitute a distinct clade (Fig. 1). This suggests the existence of a new group within Stellaria. Notably, S. pentastyla and S. procumbens share morphological similarities (refer to Table 2) such as linear leaves, glabrous stems and 5 styles (Wang et al. 2020; Yang et al. 2020). Moreover, they have overlapping distribution (Lushui, Yunnan) and similar altitudinal distribution range (2100–3800 m). After comparing the field and specimen morphology of S. procumbens and S. pentastyla, it was found that there was no significant difference between the two. It indicates that S. procumbens and S. pentastyla are not two distinct species, but the same species. Furthermore, our phylogenetic result supports this conclusion that S. procumbens and S. pentastyla form a strongly-supported clade (BS = 100, PP = 1.00, Fig. 1). Considering the publication date of S. pentastyla (4 March 2020) preceding that of S. procumbens (9 March 2020), we propose that S. procumbens should be treated as a new synonym of S. pentastyla according to the Art. 11. 4 of the Shenzhen Code (Turland et al. 2018).

Having five or more lobes per petal is an exceptional character state in Stellaria, with Stellaria radians L. as the only species exhibiting this trait (Chen and Rabeler 2001). Despite its unique floral morphology, S. radians is widely recognised as a member of Stellaria (Schischkin 1970; Wu and Ke 1996; Chen and Rabeler 2001). Previous phylogenetic studies also indicated that it was nested in core Stellaria and formed an Insignes clade with other Stellaria species (Sharples and Tripp 2019). Our results revealed that S. multipartita is another species of Stellaria which possesses ten or more lobes per petal because it formed a clade with Stellaria pubera and S. corei (Fig. 1). The previous study indicated S. radians formed a clade with S. pubera, S. corei and S. sessiliflora Y.Yabe (Sharples and Tripp 2019). It implied the close relationship between S. radians and S. multipartita. While S. multipartita shares similar petals with S. radians, it differs significantly in terms of petal characteristics (10–12-cleft vs. 5–7-cleft in S. radians) and distribution (Chongqing vs. Hebei, Heilongjiang, Jilin, Liaoning and Neimenggu in S. radians). This difference, as well as our phylogenetic data, support the treatment of S. multipartita as a new Stellaria species.

Taxonomic conclusions

Stellaria pentastyla W.Qiao Wang, H.F.Xu & Z.H.Ma, Phytotaxa 435: 71. [4 March] 2020. Type: CHINA. Yunnan: Lushui, elev. ca. 3102 m, 25°58'26"N, 98°40'44"E, 8 June 2017, Xu & Mou YN0014 (holotype GAUA!, isotypes IBSC!)

= Stellaria procumbens Huan C.Wang & Feng Yang, Phytotaxa 435: 195. [9 March] 2020. Type: CHINA. Yunnan Province: Luquan County, Zhuanlong Town, Jiaozishan National Nature Reserve, 26°04'58"N, 102°51'04"E, elev. 3380 m, 12 July 2019, H. C. Wang et al. LQ 7217 (holotype YUKU!, isotypes YUKU!), syn. nov.

Schizotechium motuoensis (Li & Song) W.Q.Wang & Z.H.Ma, comb. nov.

urn:lsid:ipni.org:names:77352937-1

≡ Stellaria motuoensis Meng Li & Y.F.Song, Nordic J. Bot. 2022(9)-e03683: 2. 2022. Type: China, Xizang, Motuo County, Mt Doxong La, Xiaoyandong, ca. 2650 m a.s.l., 95°04'10.33"E, 29°24'51.13"N, 22 October 2021, Meng Li 3021 (holotype: NF, isotypes: CDBI).

Stellaria longipedicellata W.Q.Wang & Z.H.Ma, sp. nov.

urn:lsid:ipni.org:names:77352938-1
Fig. 2

Type

China • Sichuan: Luding, growing on scree slopes, elev. ca. 2881 m, 29°51'49.2"N, 102°17'23.0"E, 8 July 2022, W.Q. Wang et al. QSC0009 (holotype GAUA!).

Figure 2. 

Morphology of S. longipedicellata A habitat B habit C habit D inflorescence (cymes) E stem F inflorescence (solitary) G leaf H flower (style 3, rarely 4) I capsule.

Diagnosis

S. longipedicellata is similar to S. decumbens in having a prostrate life form and few-flowered cymes or solitary flowers, but differs from the latter by having glabrous stems (vs. densely pilose stems), linear-lanceolate leaves (vs. oblong leaves), 1.2–2 cm pedicel, longer than sepals (vs. ca. 4 mm or less pedicel, shorter than or equalling sepals) and petals slightly shorter than or sub-equalling petals (vs. petals ca. 1/2 as long as sepals, in Table 2).

Description

Perennial herbs, whole plants glabrous. Stems, slender, prostrate or slightly ascending, much branched, 5–10 cm tall. Leaves sessile, green, linear-lanceolate, minute, 3–7 mm long, 0.6–1 mm broad, apex acute. Inflorescence axillary or terminal, 1–3-flowered. Pedicel 1.2–2 cm, slender. Bracts lanceolate, 3–4 mm, margin membranous. Sepals 5, glabrous, lanceolate, 4–5 mm long, 0.8–1 mm broad, margin membranous, apex acuminate. Petals 5, slightly shorter than or subequalling sepals, deeply bifid. Stamens 10, slightly shorter than or subequalling petals. Styles 3, rarely 4, filiform. Capsule ovoid-cylindrical, slightly longer than or subequalling persistent sepals. Seeds numerous, red-brown, ovoid, conspicuously rugulose.

Phenology

Flowering time June–July, fruiting time August–September.

Distribution and ecology

It is only known from the type locality, growing on scree slopes.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This work is supported by National Natural Science Foundation of China (Grant No. 32260047 and 31970220) and Natural Science Foundation of Guangxi Province (Grant No. 2023GXNSFAA026346).

Author contributions

Writing - original draft: Wenqiao Wang. Writing - review and editing: Zhonghui Ma, Zhiwei Su.

Author ORCIDs

Wenqiao Wang https://orcid.org/0000-0002-8946-6995

Zhiwei Su https://orcid.org/0000-0003-2998-8617

Zhonghui Ma https://orcid.org/0000-0002-3898-3079

Data availability

All of the data that support the findings of this study are available in the main text or Supplementary Information.

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Supplementary material

Supplementary material 1 

List of taxa sampled and GenBank accession numbers of sequences used in phylogenetic analyses of Alsineae

Wenqiao Wang, Zhonghui Ma

Data type: xlsx

Explanation note: This is a table including GenBank accession numbers of sequences used in phylogenetic analyses of Alsineae.

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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