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Research Article
Begonia parvibracteata, a new species in Begonia sect. Platycentrum (Begoniaceae) from Guangxi of China, based on morphological and molecular evidence
expand article infoXin-Xin Feng‡, Xiao-Feng Huang‡, Yu-Ni Huang‡, Zhi-Xian Liu‡, Ren-Kun Li§, Jin-Ye Zhou|, Wei Guo, Xiao-Yan Chen#, Dai-Ke Tian¤«
‡ Dongguan Botanical Garden, Dongguan, China
§ Enshi Dongsheng Plant Development Co. Ltd., Enshi, China
| Flower Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, China
¶ Zhongkai University of Agriculture and Engineering, Guangzhou, China
# Guangdong Joco Eco-Environment Co., Ltd, Dongguan, China
¤ Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China
« Shanghai Key Laboratory for Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai, China

Corresponding author: Xiao-Feng Huang ( 1037758218@qq.com )

Corresponding author: Dai-Ke Tian ( dktian@cemps.ac.cn )

Academic editor: Jan Wieringa
© 2022 Xin-Xin Feng, Xiao-Feng Huang, Yu-Ni Huang, Zhi-Xian Liu, Ren-Kun Li, Jin-Ye Zhou, Wei Guo, Xiao-Yan Chen, Dai-Ke Tian.
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: Feng X-X, Huang X-F, Huang Y-N, Liu Z-X, Li R-K, Zhou J-Y, Guo W, Chen X-Y, Tian D-K (2022) Begonia parvibracteata, a new species in Begonia sect. Platycentrum (Begoniaceae) from Guangxi of China, based on morphological and molecular evidence. PhytoKeys 214: 27-38. https://doi.org/10.3897/phytokeys.214.90004
Open Access

Abstract

The previously reported begonias in a limestone forest of Guangxi mainly belong to Begonia sect. Coelocentrum Irmscher. In this article, we described and illustrated a new species in sect. Platycentrum (Klotzsch) A.DC., Begonia parvibracteata X.X.Feng, R.K.Li & Z.X.Liu, which was discovered in a karst forest of south-western Guangxi. The begonia shows high morphological similarity to B. subhowii S.H. Huang and B. psilophylla Irmscher, but differs from the latter two in its narrower oblique-ovate asymmetric leaf blade, 4 (occasionally 6) tepals of pistillate flower and smaller membranous inflorescence bracts. Molecular phylogenetic analysis, based on ITS sequence data, supports the new species as monophyletic and distinct from B. subhowii and B. psilophylla. Considering its narrow distribution and the disturbance of human activities, the conservation status of new taxon is evaluated as “Vulnerable” (VU B1, B2 ab (i, iv, v), D2) according to the IUCN Red List Categories and Criteria.

Keywords

ITS, morphology, new taxon, southern China, taxonomy

Introduction

According to the latest report, China’s wild begonias have already increased to 239 species (iBegonia 2021). The total number of species could reach 300 in the coming years, meeting the prediction of Tian et al. (2018). Consisting of 122 species, Sect. Platycentrum (Klotzsch) A.DC. represents the largest section of Begonia in China, with 66 species mainly distributed in Yunnan. Eighty-seven species of Begonia have so far been found in Guangxi (iBegonia 2021), most of which (60 species) are distributed in the karst forest and belong to B. sect. Coelocentrum Irmscher.

In Guangxi, only 11 species belong to B. sect. Platycentrum (Klotzsch) A.DC., and six of which are widespread in south and southeast China: B. circumlobata Hance, B. edulis Lévl., B. handelii Irmsch., B. hemsleyana Hook.f., B. longiciliata C.Y.Wu and B. longifolia Blume. Only five species of B. sect. Platycentrum are endemic to Guangxi, including B. tsoongii C.Y.Wu (Wu and Ku 1995), B. longanensis C.Y.Wu (Wu and Ku 1997), B. aurora C.I Peng, Yan Liu & W.B. Xu (Liu et al. 2020), B. scorpiuroloba D.K.Tian & Q.Tian (Tian et al. 2021) and B. pseudoedulis D.K.Tian, X.X.Feng & R.K.Li (Feng et al. 2021).

An unknown Begonia taxon with reproductive organs was collected from Guangxi during our field survey and plant collection in May 2020 and October 2021, respectively. The begonia definitely belongs to B. sect. Platycentrum, but differs markedly from the reported 11 begonias of the same section in Guangxi. After further detailed morphological observation, morphological comparison with similar species and molecular analysis, it is confirmed as a new species in Begonia sect. Platycentrum.

Materials and methods

Taxonomic observation

Morphological characters were observed and measured from fresh samples in the field. Morphological comparisons with similar taxa were undertaken by consulting the literature, examining herbarium (IBK and IBSC) specimens and observing living collections cultivated in the nursery of Enshi Dongsheng Plant Development Co. Ltd. The specimens were deposited at the South China Botanical Garden (IBSC), CAS and Chenshan Herbarium (CSH) of Shanghai Chenshan Botanical Garden.

DNA sequencing and molecular analysis

The fresh leaves of the putative new species and the morphologically similar allied species, B. subhowii and B. psilophylla, were collected in the field and the nursery, respectively. Total DNA was extracted from nine individuals of the three species (B. parvibracteata, B. subhowii and B. psilophylla) with the CTAB method (Doyle and Doyle 1987). The internal transcribed spacers 1 and 2 (ITS) and the 5.8S gene were amplified using the primers 17SE and 26SE (Forrest and Hollingsworth 2003). PCR amplification and Sanger sequencing were performed according to Fan et al. (2014), with an annealing temperature of 53 °C. The ITS sequences of the three species were uploaded to GenBank (http://www.ncbi.nlm.nih.gov/) with the accession numbers OL892048, OL892049 and OL892050 for B. parvibracteata sp. nov., OL871361, OL871362 and OL871363 for B. subhowii and OL851701, OL851702 and OL851703 for B. psilophylla (Table 1).

Table 1.
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Begonia species and populations included in the phylogenetic analysis (Sectional placement follows Moonlight et al. 2018).

Taxon Origin GenBank accession no. Section Collector, voucher (Herbarium)
Begonia acetosella Craib. Mengla, Yunnan, China MW690106 Platycentrum Wang, W.G., WWG005 (HITBC)
Begonia biflora Ku Malipo, Yunnan, China JF975965 Coelocentrum Shui, Y.M. et al. 20484 (KUN)
Begonia chingii Irmsch. Napo, Guangxi, China KP710820 Reichenheimia Tian, D.K., Li, C. TDK785 (CSH)
Begonia circumlobata Hance Xinyi, Guangdong, China KP710815 Platycentrum Tian, D.K., Li, X.P. TDK866 (CSH)
Begonia cucurbitifolia C. Y. Wu Yunnan,China JF975969 Platycentrum Y,M,Shui et al.GBOWS1284 (KUN)
– JF975968 –
Begonia edulis Lévl. Bama, Guangxi, China KP710813 Platycentrum Tian, D.K., Li, C. TDK757 (CSH)
Begonia grandis Dry. Yongshun, Huhan, China KP710828 Diploclinium Li, X.P. Li, X.J. LXJ022 (CSH)
Begonia handelii Irmsch. Fengshan, Guangxi, China KP710818 Platycentrum Tian, D.K., Li, C. TDK763 (CSH)
Begonia hatacoa Buch.-Ham. ex D. Don – AF485111 Platycentrum –
Begonia hemsleyana Hook. f. – KP710806 Platycentrum –
Begonia henryi Hemsl. Leshan, Sichuan, China KP710822 Reichenheimia Tian, D.K., Tian, L.Z. TDK2249 (CSH)
Begonia huangii Y. M. Shui & W. H. Chen Gejiu, Yunnan, China JF976001 Coelocentrum Shui, Y.M. et al. 40782 (KUN)
Begonia jinyunensis C. I Peng, B. Ding & Q. Wang Jinyunshan, Chongqing, China MZ145345 Platycentrum –
Begonia labordei Lévl. Yunnan, China KF636452 Diploclinium Peng 20520 (HAST)
Begonia longifolia Blume Mengla, Yunnan, China MW690102 Platycentrum Wang, W.G., WWG001 (HITBC)
Begonia longistyla Y. M. Shui & W. H. Chen Hekou, Yunnan, China JF976018 Coelocentrum Shui, Y.M. et al. 40778 (KUN)
Begonia megalophyllaria C. Y. Wu Yunnan, China JF976026 Platycentrum Y,M,Shui et al.D-33(KUN)
Begonia multangula Blume Jawa, Lesser Sunda Is. MN453434 Platycentrum –
Begonia ornithophylla Irmsch. Guangxi, China JF976032 Coelocentrum Y,M,Shui et al. B2005-061(KUN)
Begonia parvibracteata X.X.Feng, R.K.Li & Z.X.Liu Longzhou, Guangxi, China OL892048 Platycentrum Xin Xin Feng, et al. 835307 (IBSC)
OL892049
OL892050
Begonia pedatifida Lévl. Tianlin, Guangxi, China KP710810 Platycentrum Tian, D.K., Li, C. TDK774 (CSH)
Begonia psilophylla Irmsch. Hekou, Yunnan, China OL851701 Platycentrum –
OL851702 –
OL851703 –
Begonia pulchrifolia D.K.Tian & C.H.Li Meinvfeng, Leshan, Sichuan, China KP710811 Platycentrum Tian, D.K., et al. TDK2243 (CSH)
Begonia scorpiuroloba D.K.Tian & Q.Tian Fanchenggang, Guangxi, China MZ145351 Platycentrum Tian, D.K., et al.TDK2269(CSH)
Begonia socotrana Hook.f. Socotra AF469121 Peltaugustia –
Begonia subhowii S. H. Huang Malipo, Yunnan, China OL871361 Platycentrum –
OL871362 –
OL871363 –

We chose 17 species from sect. Platycentrum and 8 species from other sections of Begonia native to mainland China to place the new species in a phylogenetic context (Table 1). Begonia socotrana Hook.f in sect. Peltaugustia (Warb.) Barkley from Socotra (for the coast of Africa) was selected as an out-group in the phylogenetic analysis (Moonlight et al. 2018). Except for the nine individuals of the putative new species and its two allied species, the additional ITS sequences for 23 Begonia species were downloaded from the NR database of NCBI. All these sequences were aligned using BioEdit v.7.2.5 (Hall 1999) and a phylogenetic analysis using Bayesian Inference (BI) was undertaken in MrBayes v.3.1.2 (Ronquist and Huelsenbeck 2003). The GTR+G model was chosen as the optimal model of nucleotide substitution according to the Akaike Information Criterion (AIC; Burnham and Anderson 2002) as implemented in MrModeltest 2.3 (Nylander 2004). The Markov chains were run for 1,000,000 generations and sampled at each 100 generations, with the first 25% discarded as burn-in.

Taxonomy

Begonia parvibracteata X.X.Feng, R.K.Li & Z.X.Liu, sp. nov.

urn:lsid:ipni.org:names:77308553-1
Figs 1, 2 Chinese name: 小苞秋海棠

Type

China Guangxi, Longzhou County (龙州县), Zhubu Town (逐卜乡), Bannong Village (板弄屯), Yinghuagu Tourist Resort, 22°33'51"N, 106°57'03"E, (Fig. 3), 263 m alt., in shaded environment of limestone forest, October, 2021, Xin-Xin Feng, Ren-Kun Li & Zhi-Xian Liu (holotype: 835307, IBSC!; isotype: SYS!). Longzhou County (龙州县), Zhubu Town (逐卜乡), Pona Village (坡那屯), Nonggang National Nature Reserve, 22°39'03"N, 106°57'18"E, 190 m alt., on rock under limestone forest, 18 May 2020, Dai-Ke Tian & Jinye Zhou TDK4119 (CSH!).

Figure 1. 

Begonia parvibracteata drawn by Yunxiao Liu A хabit B staminate inflorescence C, D front and back views of staminate flower E lateral view of staminate flower F stamen G, H front and back views of pistillate flower with 4 tepals I front view of pistillate flower with 6 tepals J cross section of ovary K styles and stigmas L stigmas M abaxial view of capsule showing wings N lateral view of capsule showing two shorter wings.

Figure 2. 

Habitat and morphology of Begonia parvibracteata A habitat B flowering plant C creeping rhizome D shoot top with stipule E leaf blade (adaxial) F, G leaf blade (abaxial) H erect stem with inflorescence I, J young inflorescence and bract; K, L front and back views of staminate flower with 4 tepals M lateral view of staminate flower N stamens O, P front and back views of pistillate flower with 4 tepals Q front view of pistillate flower with 6 tepals R cross section of ovary S stigmas T, U immature capsule V dried mature capsule (Photos by Z.X. Liu).

Figure 3. 

Distribution of B. parvibracteata, B. subhowii, B. psilophylla and B. cucurbitifolia.

Diagnosis

Begonia parvibracteata morphologically resembles B. subhowii and B. psilophylla in rhizome and leaf characters. However, it has narrowly oblique-ovate asymmetric leaf blades, 4 (rarely 6) tepals in pistillate flowers and small (6–8 × 3–5 mm) bracts in inflorescences. These characters differ from the widely ovate leaf blades, 5 (rarely 6) tepals of pistillate flowers, and distinctly large bracts in inflorescences of B. subhowii. B. parvibracteata is dissimilar to B. psilophylla in its 4 (rarely 6) tepals in pistillate flowers and asymmetric, narrowly oblique-ovate leaf blade.

Begonia parvibracteata forms a monophyletic group clustered with B. cucurbitifolia in the phylogenic tree, but the latter has nearly symmetric, 3–4 lobed leaf blade, 5-tepaled pistillate flower, definitely differing from the new species.

Description

Perennial evergreen herb, monoecious, 15–30 cm tall. Rhizome creeping, ca. 8.5–12 cm long and 6–10 mm thick, internode short or not obvious; erect stem only seen at anthesis, ca. 7.5–10 cm long, internodes 1–2 (3), green to reddish-green, glabrous. Stipules brownish-red, translucent, ovate-triangular, ca. 8–10 × 4–5 mm, glabrous. Leaves 3–6 basal and 2–3 aerial, petiole yellowish-green, 18–22 cm long, glabrous; blade asymmetric, ovate to narrowly ovate, 14–16 × 7.5–9 cm; apex acuminate to caudate, base oblique-cordate; leaf margin usually almost entire or occasionally crenate; venation palmate with 6–8 primary veins, adaxially slightly concave, abaxially convex; leaf blade fleshy, abaxially pale-green, glabrous; adaxially green, glabrous. Inflorescences arising from erect stem; dichasial cymes branching one to two times, peduncle 10–12 cm long, glabrous; flowers unisexual, 3–7 flowers per inflorescences; bracts membranous, triangular to widely ovate, brownish-red, 6–8 × 3–5 mm, glabrous. Staminate flower: pedicels pale green, ca. 2–2.3 cm long, glabrous; tepals 4, outer 2 tepals ovate to circular, 13–21 × 12–20 mm, adaxially concave, pinkish-white, abaxially convex, pinkish-white, red hispid; inner 2 obovate, 10–18 × 8–12 mm, margin irregularly entire, white, glabrous; androecium cylindrical, ca. 6.6–7.5 mm across; stamens numerous, ca. 2–2.5 mm long, anthers yellow, clavate, base cuneate, ca. 1.5 mm long. Pistillate flower: pedicels pale green, ca. 2–2.6 cm long, glabrous; tepals 4, occasionally 6, white, irregularly ovate, obovate or cuneate, sub-equal, 18–20 × 10–15 mm, glabrous; ovary yellowish-green, trigonous-ellipsoid, 11–12 × 5–6 mm (wings excluded), glabrous; 2-loculed, placentae axillary, placentae bifid per locule; styles 2, fused at base, yellow, ca. 5–6 mm long, apically Y-shaped, stigma U-shaped, spirally twisted. Capsules nodding, trigonous-ellipsoid, ca. 11–13 × 5–6.5 mm (wings excluded), yellowish-green, glabrous, unequally 3-winged, abaxial wing triangular to ligulate, ca. 10–13 mm long; lateral wings lunate, 3–6 mm long.

Distribution and habitat

Currently known from four localities in Longzhou County and Daxin Countym Guangxi, China. It usually grows on rocks or rock cracks in limestone under forest.

Phenology

Flowering September-October, fruiting October-December.

Etymology

The specific epithet “parvibracteata” refers to the short small bracts of the new species. The Chinese name is given as “小苞秋海棠” (Begonia with small inflorescence bracts).

Conservation status

There are three populations with approximately 1000 individuals found in Longzhou County. Another one population with approximately 500 individuals is distributed in the Encheng National Nature Reserve, Daxin County. Some plants of this begonia are over-collected and sold in the local medicinal herb market of Longzhou County. According to the IUCN Red List Categories and Criteria (IUCN 2022), B. parvibracteata should be assessed as “Vulnerable (VU B1, B2 ab (i, iv, v), D2)” due to its narrow distribution and the disturbance by human activities.

Molecular analysis

The aligned matrix of the ITS sequence data was 727 bp long. The result of Bayesian Inference analysis is shown in Fig. 4. Begonia sect. Platycentrum appears monophyletic with a high Bayesian posterior probability (bpp = 1) (Fig. 4). The three samples of the putative new species form a monophyletic group clustered with B. cucurbitifolia (bpp = 0.89). Begonia subhowii with the highest morphological similarity to B. parvibracteata formed another subclade.

Figure 4. 

Bayesian Inference of the phylogenetic position of the newly-described B. parvibracteata within sect. Platycentrum, based on nuclear ITS sequences.

The nodes with bpp < 0.50 have been collapsed. Sectional placement of taxa is indicated by the following abbreviations: Coe (Coelocentrum), Dip (Diploclinium), Pla (Platycentrum), Rei (Reichenheimia) and Pel (Peltaugustia). The numbers after the species names indicate different populations. The samples of the new species are marked with stars.

Discussion

The new begonia with 2-loculed ovary, axillary placentation and bifid placentae can be clearly assigned to B. sect. Platycentrum (Gu et al. 2007). Within this largest section for Begonia in China, B. parvibracteata shows high morphological resemblance to B. subhowii and B. psilophylla, both of which are distributed in south-eastern Yunnan (Shui and Huang 1999; Shui and Chen 2018), including creeping rhizome, glabrous plants with both basal and cauline leaves at anthesis, usually almost entire leaf margin, palmate venation, fleshy green leaf blade and 4 tepals of staminate flower (Table 2).

Table 2.
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Morphological comparison of B. parvibracteata and relevant taxa.

Character B. subhowii B. psilophylla B. cucurbitifolia B. parvibracteata
Leaf blade shape asymmetric, widely ovate nearly symmetric, widely ovate to cordate nearly symmetric, orbicular, 3–4 lobed asymmetric, narrowly oblique-ovate
Leaf blade base asymmetric, oblique-cordate nearly symmetric, obtuse nearly symmetric, cordate asymmetric, oblique-cordate
Leaf margin irregularly serrulate minutely serrulate minutely serrulate usually almost entire or occasionally crenate
Inflorescence bracts ovate-oblong, 50 × 30 mm, glabrous, apex acuminate elliptic to ovate-oblong, 7–9 × 4–5 mm, glabrous subglabrous, caduceus triangular, 6–8 × 3–5 mm, glabrous
Tepal number of pistillate flowers usually 5, rarely 6 usually 5, rarely 6 5 usually 4, rarely 6
Phenology (flowering; fruiting) April-May; May-July February-March; March-May July-August; August-October September-October; October-December
Habitat 700–1500 m alt., limestone, Yunnan; Vietnam 100–700 m alt., limestone, Yunnan 430 m alt., limestone, Yunnan 263 m alt., limestone, Guangxi

In B. subhowii, there are 5 (occasionally 6) tepals in the pistillate flower and the bracts of inflorescence is distinctly long and large (5 × 3 cm) (Fig. 5). These characters differ from 4 (occasionally 6) tepals and triangular to widely ovate (6–8 × 3–5 mm) bracts in B. parvibracteata. In addition, the leaf blade is wider ovate in B. subhowii, compared with the narrower oblique-ovate shape of B. parvibracteata.

Figure 5. 

B. subhowii A–I B. psilophylla J–L B. cucurbitifolia M, N showing similar features comparable to B. parvibracteata A habitat B young leaf blade (adaxial) C leaf blade (abaxial) D inflorescence E bracts F, G front and back views of staminate flower H front view of pistillate flower with 5 tepals I lateral view of pistillate flower J flowering plant K symmetric leaf blade L front view of flower M leaf blade of juvenile plant N mature leaf blade (Photos A–I by R.K. Li J–L by Z.X. Liu M, N by D.K. Tian).

In B. psilophylla, the leaf blade is nearly symmetric, widely ovate with symmetric cordate base, in contrast with the narrower ovate leaf blade and oblique-cordate base of the new species. Furthermore, there are 5 (occasionally 6) tepals in the pistillate flower of B. psilophylla, being different from the 4 (occasionally 6) tepals of B. parvibracteata.

According to the phylogenetic tree, based on ITS sequences, the closest relative of B. parvibracteata is B. cucurbitifolia which is also distributed in south-eastern Yunnan. However, B. cucurbitifolia is remarkably distinct from B. parvibracteata in morphology, including nearly symmetric, 3–4 lobed leaf blade and 5-tepaled pistillate flower.

For the flowering time, B. parvibracteata blooms later compared with its three allied species mentioned above.

Acknowledgements

This study was supported by the Guangdong Rural Revitalization Strategic Foundation (20211800400042), the Dongguan Municipal Project for Improvement of Social Science and Technology (2020507101165; 2016108101018), the Dongguan Sci-tech Commissioner Program (Grant No. 20221800500042) and the Guangzhou Science and Technology Program (201903010076). We are also grateful to the editor, the reviewers and the English corrector for improving our manuscript.

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