Botanical Studies

An International Journal

Impact Factor 1.159

Botanical Studies Cover Image
Open Access

Begonia myanmarica (Begoniaceae), a new species from Myanmar, and molecular phylogenetics of Begonia sect. Monopteron

Botanical StudiesAn International Journal201758:21

DOI: 10.1186/s40529-017-0175-9

Received: 29 November 2016

Accepted: 30 March 2017

Published: 7 April 2017

Abstract

Background

A new species, Begonia myanmarica, was discovered from Myanmar and herein documented. Characterized by a single developed wing in the ovary/fruit, this species would be assigned to sect. Monopteron (sensu Doorenbos et al. in The sections of Begonia including descriptions, keys and species lists: studies in Begoniaceae VI. Wageningen Agricultural University, Wageningen, 1998) that is known by B. griffithiana and B. nepalensis from the Himalaya. To confirm its sectional assignment, we conducted morphological, phylogenetic and cytological studies.

Results

Morphological observations indicated that B. myanmarica was distinguishable from the two known species of sect. Monopteron by the leaf shape and size, 1-locular ovary, parietal placentation and chromosome number. Molecular phylogenetic analysis using nrITS sequences showed that B. myanmarica was not allied with the clade of sect. Monopteron, though both were nested within sect. Platycentrum-sect. Sphenanthera clade.

Conclusions

Studies of morphology, molecular phylogenetics and cytology support the recognition of the new species, Begonia myanmarica, which is fully described and illustrated. Our results also indicate that B. myanmarica is not closely related to species previously assigned to sect. Monopteron, suggesting that the fruit morphology of a single developed wing in the ovary/fruit characterizing sect. Monopteron is homoplasious.

Keywords

Begonia griffithiana Begonia nepalensis Chromosome Morphology

Background

Begonia L. (Begoniaceae), comprising more than 1800 species classified into 68 sections (Doorenbos et al. 1998; Hughes et al. 2015; Christenhusz and Byng 2016), is one of the largest genera of vascular plants. With more than 760 Begonia species in Asia, Doorenbos et al. (1998) recognized 18 sections [Alicida C.B. Clarke, Apterobegonia Warb., Baryandra A. DC., Bracteibegonia A. DC., Coleocentrum Irmscher, Diploclinium (Lindl.) A. DC., Haagea (Klotzsch) A. DC., Heeringia Irmscher, Lauchea (Klotzsch) A. DC., Monophyllon A. DC., Monopteron (A. DC.) Warb., Parvibegonia A. DC., Petermannia (Klotzsch) A. DC., Platycentrum (Klotzsch) A. DC., Putzeysia (Klotzsch) A. DC., Reichenheimia (Klotzsch) A. DC., Ridleyella Irmscher, and Sphenanthera (Hassk.) Warb.]. Thereafter, four additional Asian sections were proposed [Leprosae (T.C. Ku) Y.M. Shui, Monolobium T.C. Ku, Pleiothece T.C. Ku, and Symbegonia (Warb.) G. Forrest & Hollingsw.] (Ku 1999; Shui et al. 2002; Forrest and Hollingsworth 2003; Ku et al. 2007). These 22 Asian sections are highly unequal in species numbers: eight of the large sections (Petermannia, Platycentrum, Diploclinium, Reichenheimia, Coleocentrum, Parvibegonia, Sphenanthera, and Symbegonia) comprise 95% of Asian Begonia species and the rest 14 sections each with less than five species (Thomas 2010). Several molecular phylogenetic studies have demonstrated the paraphyly or polyphyly of these large sections, suggesting homoplasy of morphological characters used for current sectional delimitations (Tebbitt et al. 2006; Thomas et al. 2011; Chung et al. 2014). However, few studies have tested the monophyly of small Asian section of Begonia thus far [but see Rajbhandary (2010); Rubite (2010); Thomas (2010)].

Myanmar is botanically a most interesting country, but there have been no critical floristic surveys for nearly half a century. Thus far about 60 species of Begonia have been recorded from Myanmar (Hughes 2008; Tanaka and Hughes 2007; Tanaka and Hayami 2011; Peng et al. 2014b; Tanaka and Peng 2016). During the fieldwork in western Myanmar on 2 February 2012, the second author (YDK) collected an unknown Begonia with only one developed wing in ovary/fruit, which is the key character of Begonia sect. Monopteron sensu Doorenbos et al. (1998) first delimited by de Candolle (1864) as Mezierea sect. Monopteron. Presently, only two species, B. griffithiana Warb. and B. nepalensis Warb., are recognized in sect. Monopteron (de Candolle 1864; Doorenbos et al. 1998). Begonia nepalensis, the type species of sect. Monopteron, is native to Bhutan, Nepal and India (Fig. 5; Doorenbos et al. 1998; Hughes et al. 2015). Its chromosome number was reported to be 2n = 16 (Legro and Doorenbos 1971), with an uncertain chromosome count 2n = 28–42 by Sharma and Bhattacharyya (1961). Begonia griffithiana, occurring in Bhutan and India (Fig. 5), is characterized by lanceolate to oblong leaves with subcordate base. Chromosome number of B. griffithiana was documented as 2n = 22 (Doorenbos et al. 1998). Based on recent systematics and phylogenetics of Begonia, sect. Monopteron is nested within the Platycentrum-Sphenanthera clade (Rubite 2010; Thomas 2010; Rajbhandary et al. 2011; Leong 2017).

Although morphology of the 1-winged ovary/capsule of the undescribed Begonia should be assigned to sect. Monopteron, it differs from B. griffithiana and B. nepalensis significantly the leaf shape, leaf size and distribution. In this study, we described it as a new species. We also provide detailed morphological data and molecular phylogenetic analysis to elucidate the sectional assignment for this species.

Methods

Morphological observations

Rhizomes of Begonia myanmarica collected by YDK from Myanmar were cultivated in the experimental greenhouse of the Biodiversity Research Center, Academia Sinica, Taipei, Taiwan. Fully grown plants with flowers and fruits (Peng 23565, 23566) were used for morphological observation. The two species of sect. Monopteron, B. griffithiana (Peng 20851) and B. nepalensis (Peng 20854), cultivated in the greenhouse were also studied as a comparison.

Chromosome preparations

Root tips were obtained from cultivated materials from greenhouse of Academic Sinica. Somatic chromosome of the new species, B. myanmarica (Peng 23566), and two species of sect. Monopteron: B. griffithiana (Peng 20851) and B. nepalensis (Peng 20854), were examined using root tips following the methods by Peng et al. (2014a).

Phylogenetic analyses

DNA sequences of the nuclear ribosomal internal transcribed spacer (nrITS) were used to evaluate the phylogenetic relationship among new species and the two species of sect. Monopteron. DNA extraction, PCR amplification and DNA sequencing followed Chung et al. (2014). To test the monophyly of sect. Monopteron and sectional assignment of new species, nrITS of 96 species used in Chung et al. (2014) were adopted for phylogenetic analysis (see Appendix for details). Alignment was conducted using MUSCLE implemented in MEGA5.2 (Tamura et al. 2011) and verified in Mesquite v3.03 (Maddison and Maddison 2015). Phylogenetic relationships were constructed by Bayesian Inference (BI) method. The best nucleotide substitution models were determined by Modeltest v2.7 (Posada and Crandall 1998). For BI analysis, the consensus topology was based on Markov chains algorithm implemented in MRBAYES 3.0b4 (Huelsenbeck and Ronquist 2001). Four chains of Markov chain Monte Carlo (MCMC) simulation were carried out for 1,500,000 generations each with trees sampled per 500 generations. The first 500 trees of sampled trees were discarded before the node probability was calculated (posterior probability: PP).

Taxonomic treatment

Begonia myanmarica C.-I Peng & Y. D. Kim, sp. nov. (Figs. 1, 2)
Fig. 1

Begonia myanmarica C.-I Peng & Y. D. Kim. A Habit. B Leaf adaxial surface. C Stipule. D Male flower, face view, D′ Male flower, side view. E, E′, E″, E‴ Stamen. F Female flower, face view, F′ Female flower, side view. G Style and stigma. H, H′, H″, H‴ Cross section of ovary. I Capsule

Fig. 2

Begonia myanmarica C.-I Peng & Y. D. Kim. a Habit and habitat. b Cultivated plant at anthesis. c Leaf abaxial view. d Stipule. e Bract. f Male flower, face view. g Male flower, side view. h Female flower, face view. i Female flower, side view. j Cross section of ovaries. k Capsule

Type

MYANMAR. Sagaing Region, Alangdaw Kathapa National Park, 22°18′ 47.7″ N, 94°28′32.7″ E, alt. 438 m, mixed deciduous forest, along the stream. Living collection made by Seong-hyun Cho, Young-dong Kim, Yong-in Kim & Jeong-hun Lee MM-0611, 2 Feb 2012; type specimens (with flowers and fruits) pressed from plants cultivated in the experimental greenhouse, Academia Sinica, Taipei, Taiwan, 20 Mar 2016, Ching-I Peng 23566 (holotype: RAF; isotypes: HAST, KB).

Diagnosis

Begonia myanmarica is a unique species with an erect habit; large, ovate to broadly ovate leaves (ca. 20–40 cm long, 22–30 mm across); sole, much protruded wing in ovary/fruit; 1-locular ovary with parietal placentation and 2 placentae; and the somatic chromosomes are determined as 2n = 38.

Herbs monoecious, perennial. Rhizomes stout, 2–4 cm across, to 9 cm long; erect stem 50–90 cm tall, 1–2 cm thick, internodes 5–15 cm, glabrous. Stipules caducous, glabrous, triangular, apex aristate or apiculate, margin entire, 7–15 mm long, 6–15 mm wide. Leaves alternate, green with slightly paler veins; petiole 20–40 cm long, 2.2–3 cm across, glabrous; leaf blade fleshy, asymmetric, ovate to broadly ovate, 21–35 cm long, 15–28 cm wide, upper surface glabrous, underside slightly hairy on veins, base obliquely cordate, margin irregularly loosely serrulate or denticulate, apex acute or short acuminate; venation 7-or 8-palmate. Inflorescence mainly terminal but also axillary racemes of dichasial cymes, bisexual, protandrous; cyme 10–15 cm long, with 2 female flowers at apex and 7–9 male flowers at base, peduncle 2–5 cm long, glabrous; bracts deciduous, ovate to triangular, apex acuminate, margin entire, 0.7–1.5 cm long, 0.4–0.6 cm wide. Male flower: pedicel 2–2.8 cm long, glabrous; tepals 4, white to pinkish, outer 2 ovate or orbicular, 1.9–2.3 cm long, 1.5–2 cm wide, inner 2, broadly oblong, 1.8–2.3 cm long, 0.5–1.5 cm wide, glabrous; androecium actinomorphic, subglobose, ca. 0.7 cm across, stamens 60–80, yellow, clavate; filaments ca. 2 mm long, fused to a short central column; anthers 1–1.2 mm long, apex truncate. Female flower: pedicel 1.7–3.5 cm long, glabrous; ovary white, wings 3, manifestly unequal, 2 side wings almost undeveloped, abaxial wing much protruded, white to pale greenish or pinkish, 1-locular; placentation parietal, placentae 2, each bilamellate; tepals 5, white in the greenhouse (pinkish in the wild), unequal, elliptic to obovate, 1.5–2 cm long, 0.5–1.1 cm wide, apex obtuse; styles 2, ca. 5 mm long, 2- or 3-cleft, fused at base, stigmatic band wavy-twisted and spiralled. Capsule nodding, stalk 3.5–5.5 cm long, abaxial wing triangular to rectangular, 2.4–3.8 cm tall, 2.0–2.4 cm wide, lateral two wings barely developed, rounded, 0.2–0.4 cm tall, 1.8–2.2 cm wide. Seeds barrel-shaped, 0.25–0.3 mm long.

Distribution and habit

Known only from the type locality.

Etymology

The epithet refers to Myanmar (formerly Burma) where it was discovered.

Additional specimens examined

MYANMAR. Sagaing Region: Alang Daw Kathapa National Park, 22°18′47.7″ N, 94°28′32.7″ E, 438 m, 2 Feb 2012, Peng 23565 (HAST); 22°18′49.5″ N, 94°28′30.2″ E, 434 m, 2 Feb 2012, MM-0556 (KB); 22°18′47.7″ N, 94°28′32.7″ E, 438 m, 2 Feb 2012, MM-0611 (KB, HHU); 22°18′44.2″ N, 94°28′28.7″ E, 380 m, 2 Feb 2012, MM-0616 (KB); 22°19′25″ N, 94°29′37.7″ E, 380 m, 5 Feb 2012, MM-0848 (KB, RAF).

Chromosome cytology

Somatic chromosome at metaphase of B. myanmarica were shown to be 2n = 38 in this study (Fig. 4c).

Discussion

Begonia myanmarica has only one developed wing in ovary/fruit (Figs. 2k, 3c, d), the key character of sect. Monopteron in Begonia (Doorenbos et al. 1998). The new species, however, deviates from sect. Monopteron with axillary placentation and two locules in ovary (Fig. 3e, f) in having 1-locular ovary and parietal placentation (Fig. 2j). Additionally, B. myanmarica has ovate to broadly ovate leaves and large leaves (ca. 20–40 cm long, 22–30 mm across) (Fig. 2b, c), whereas leaves of B. griffithiana and B. nepalensis are lanceolate to oblong and no longer than 20 × 10 cm (Fig. 3a, b). Cytologically, somatic chromosome of B. myanmarica is determined to be 2n = 38 (Fig. 4c), while chromosomes of B. griffithiana and B. nepalensis are both 2n = 16 (Fig. 4a, b) in our study. Geographically, B. myanmarica is endemic to Myanmar while B. griffithiana and B. nepalensis are distributed in India, Nepal and Bhutan (Fig. 5). We concluded that B. myanmarica is sharply distinct from B. griffithiana and B. nepalensis.
Fig. 3

Overview of leaves, fruit and cross section of ovary in Begonia griffithiana and B. nepalensis. a, b Leaves. c, d Fruit. e, f Cross section of ovary. Begonia griffithiana (a, c, e). Begonia nepalensis (b, d, f)

Fig. 4

Somatic chromosomes at metaphase of Begonia. a B. griffithiana (2n = 16, Peng 20851). b B. nepalensis (2n = 16, Peng 20854). c B. myanmarica (2n = 38, Peng 23566). Scale bar 5 µm

Fig. 5

Distribution map of Begonia griffithiana (circle), B. myanmarica (star), B. nepalensis (trangle). Distribution data of B. griffithiana and B. nepalensis is based on GPS data in the Begonia Resource Center (Hughes et al. 2015)

In our molecular phylogenetic study, B. griffithiana and B. nepalensis form a strongly supported clade (posterior probability, PP = 1) nested within the clade dominated by sect. Platycentrum-sect. Sphenanthera clade [Fig. 6; Clade PLA-SPH in Chung et al. (2014)], congruent with the studies of Rubite (2010), Thomas (2010), Rajbhandary et al. (2011), and Leong (2017). Two sampled individuals of B. myanmarica also fall within the Clade PLA-SPH but not clustered within sect. Monopteron clade (Fig. 6), suggesting that the fruit morphology of a single developed wing in the ovary/fruit is homoplasious. Morphologically, the key characters for sect. Platycentrum-sect. Sphenanthera clade are evergreen, rhizomatous and two locules in ovary (Leong 2017). Begonia myanmarica is evergreen with stout rhizome, but having 1-locular ovary. Compared with other species in sect. Platycentrum-sect. Sphenanthera, B. myanmarica is unique with a single developed wing and having 1-locular ovary not known in any other taxa in this clade. Further studies with increasing sampling of Myanmar Begonia are needed to place B. myanmarica in its proper infrageneric position.
Fig. 6

Phylogenetic tree of section Platycentrum-section Sphenanthera in Begonia generated from Bayesian analysis of nrITS sequence data. Numbers on the branches indicate posterior probability of Bayesian inference analysis. The inset is simplified phylogenetic tree based on the nrITS dataset and sectional classification of Chung et al. (2014)

Conclusion

Studies of morphology, molecular phylogenetics and cytology support the recognition of the new species, Begonia myanmarica, which is fully described and illustrated. Our results also indicate that B. myanmarica is not closely related to species previously assigned to sect. Monopteron, suggesting that the fruit morphology of a single developed wing in the ovary/fruit characterizing sect. Monopteron is homoplasious.

Declarations

Authors’ contributions

YDK, KMH, and SHC conducted the fieldwork and collected the new species from Myanmar; YDK and CIP took color photographs of B. myanmarica from the wild and the experimental greenhouse respectively; YHT carried out the morphological observation and undertook laboratory analyses; YK carried out the cytological study; YHT, CIP and KFC prepared the manuscript. All authors read and approved the final manuscript.

Acknowledgements

This work was supported by grants from the National Institute of Biological Resources (NIBR), the Ministry of Environment (MOE) of the Republic of Korea (NIBR2016 04201) and Biodiversity Research Center, Academia Sinica, Taiwan. Our gratitude extends to the Ministry of Natural Resources and Environmental Conservation of Myanmar for the continuous guidance and support for this project. We are indebted to Dr. Rekha Morris who provided research materials of B. griffithiana and B. nepalensis for cytological study; Mr. Ku-Feng Lin, manager of Academia Sinica greenhouse, for providing facilities and assistance to maintain the Begonia living collections.

Competing interests

The authors declare that they have no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
Research Museum and Herbarium (HAST), Biodiversity Research Center, Academia Sinica
(2)
Department of Life Science, Hallym University
(3)
Popa Mountain Park, Nature and Wildlife Conservation Division, Ministry of Natural Resources and Environmental Conservation
(4)
International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology

References

  1. Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261(3):201–217. doi:10.11646/phytotaxa.261.3.1 View ArticleGoogle Scholar
  2. Chung K-F, Leong W-C, Rubite RR, Repin R, Kiew R, Liu Y, Peng C-I (2014) Phylogenetic analyses of Begonia sect. Coelocentrum and allied limestone species of China shed light on the evolution of Sino-Vietnamese karst flora. Bot Stud 55:1. doi:10.1186/1999-3110-55-1 View ArticleGoogle Scholar
  3. de Candolle A (1864) Begoniaceae. In: de Candolle A (ed) Prodromus systematis naturalis regni vegetabilis. Treuffel et Würtz, Masson, pp 266–408Google Scholar
  4. Doorenbos JM, Sosef MS, de Wilde JJFE (1998) The sections of Begonia including descriptions, keys and species lists: studies in Begoniaceae VI. Wageningen Agricultural University, WageningenGoogle Scholar
  5. Forrest LL, Hollingsworth PM (2003) A recircumscription of Begonia based on nuclear ribosomal sequences. Plant Syst Evol 241(3):193–211. doi:10.1007/s00606-002-0033-y View ArticleGoogle Scholar
  6. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755. doi:10.1093/bioinformatics/17.8.754 View ArticlePubMedGoogle Scholar
  7. Hughes M (2008) An annotated checklist of Southeast Asian Begonia. Royal Botanic Garden Edinburgh, EdinburghGoogle Scholar
  8. Hughes M, Moonlight PW, Jara A, Pullan M (2015) Begonia Resource Centre. http://padme.rbge.org.uk/begonia. Accessed 15 July 2016
  9. Ku T-C (1999) Begoniaceae. In: Ku T-C (ed) Flora Reipublicae Popularis Sinicae, vol 52, no 1. Science Press, Beijing, pp 126–269Google Scholar
  10. Ku C-Z, Peng C-I, Turland NJ (2007) Begoniaceae. In: Raven PH, Hong D-Y (eds) Flora of China, vol 13., Science Press, Beijing & Missouri Botanical Garden Press, St. Louis, pp 153–207Google Scholar
  11. Legro RAH, Doorenbos J (1971) Chromosome numbers in Begonia II. Neth J Agric Sci 19:176–183Google Scholar
  12. Leong, W-C (2017) Molecular phylogenetics of Asian Begonia (Begoniaceae): systematics and biogeographic implications. PhD Dissertation, National Taiwan University
  13. Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis, version 3.03 ed. http://mesquiteproject.org. Accessed 7 Mar 2015
  14. Peng C-I, Jin X-H, Ku S-M, Kono Y, Huang H-Y, Yang H-A (2014a) Begonia wuzhishanensis (sect. Diploclinium, Begoniaceae), a new species from Hainan Island, China. Bot Stud 55:24. doi:10.1186/1999-3110-55-24 View ArticleGoogle Scholar
  15. Peng C-I, Wang H, Kono Y, Yang H-A (2014b) Begonia wui-senioris (sect. Platycentrum, Begoniaceae), a new species from Myanmar. Bot Stud 55:13. doi:10.1186/1999-3110-55-13 View ArticleGoogle Scholar
  16. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818. doi:10.1093/Bioinformatics/14.9.817 View ArticlePubMedGoogle Scholar
  17. Rajbhandary S (2010) Systematic revision of the genus Begonia L. (Begoniaceae) in the Himalayas. PhD dissertation, Tribhuvan University
  18. Rajbhandary S, Hughes M, Phutthai T, Thomas DC, Krishna KS (2011) Asian Begonia: out of Africa via the Himalayas? Gard Bull (Singapore) 63(1 & 2):277–286Google Scholar
  19. Rubite RR (2010) Systematic studies on Philippine Begonia L. secion Diploclinium (Lindl.) A.D.C. (Begoniaceae). PhD dissertation, De La Salle University
  20. Sharma AK, Bhattacharyya UC (1961) Cytological studies in Begonia II. Caryologia 14:279–301View ArticleGoogle Scholar
  21. Shui Y-M, Peng C-I, Wu C-Y (2002) Synopsis of the Chinese species of Begonia (Begoniaceae), with a reappraisal of sectional delimitation. Bot Bull Acad Sin 43(4):313–327Google Scholar
  22. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121 View ArticlePubMedPubMed CentralGoogle Scholar
  23. Tanaka N, Hayami Y (2011) Begonia kachinensis (sect. Sphenanthera, Begoniaceae), a new species from Myanmar. Acta Phytotax Geobot 61(3):151–154Google Scholar
  24. Tanaka N, Hughes M (2007) Begonia (Sect Sphenanthera) hayamiana (Begoniaceae), a new species of Begonia (Begoniaceae) from Northern Myanmar. Acta Phytotax Geobot 58(2–3):83–86Google Scholar
  25. Tanaka N, Peng C-I (2016) Begonia togashii (Begoniaceae: sect. Platycentrum), a new species from central Myanmar. Acta Phytotax Geobot 67(3):191–197. doi:10.18942/apg.201608 Google Scholar
  26. Tebbitt MC, Lowe-Forrest L, Santoriello A, Clement WL, Swensen SM (2006) Phylogenetic relationships of Asian Begonia, with an emphasis on the evolution of rain-ballist and animal dispersal mechanisms in sections Platycentrum, Sphenanthera and Leprosae. Syst Bot 31(2):327–336. doi:10.1600/036364406777585784 View ArticleGoogle Scholar
  27. Thomas DC (2010) Phylogenetics and historical biogeography of Southeast Asian Begonia L. (Begoniaceae). PhD dissertation, University of Glasgow
  28. Thomas DC, Hughes M, Phutthai T, Rajbhandary S, Rubite R, Ardi WH, Richardson JE (2011) A non-coding plastid DNA phylogeny of Asian Begonia (Begoniaceae): evidence for morphological homoplasy and sectional polyphyly. Mol Phylogenet Evol 60(3):428–444. doi:10.1016/j.ympev.2011.05.006 View ArticlePubMedGoogle Scholar

Copyright

© The Author(s) 2017