Abstract
The section Stenophora is the most basal clade in the phylogeny of the genus Dioscorea. Most of the species in the section have not been morphologically and embryologically investigated and phylogenetic relationships among species of this section are not very clear. Embryological features, such as the structure of anthers, pollen, ovules, embryo sacs etc., less undergo phenotypic variability and can be used as important characters for systematics and phylogeny. Comparative morphological and embryological analyses of the reproductive structures in 5 Dioscorea species of the section Stenophora (D. balcanica, D. caucasica, D. deltoidea, D. nipponica, D. villosa) are presented. Four characters, which may be significant for systematics of this section as well as the whole genus Dioscorea, were designated: (1) heteromorphism of the stamens in the male flower; (2) the structure of the stigma; (3) the structure of the ovule; (4) the type of female gametophyte development. It was shown that D. balcanica, D. caucasica, D. deltoidea are characterized by similar morphological features and differ from D. nipponica and D. villosa. Analysis of haplotype networks showed that the section Stenophora consists of genetically close species, that was confirmed by the phylogenetic tree of this section. The morphological similarity of D. balcanica, D. caucasica and D. deltoidea is consistent with their location on the phylogenetic tree. However, detailed morphological, embryological and molecular phylogenetic studies of a larger number of species are needed for more accurate interpretation of the Stenophora phylogenetic system.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asiedu R, Sartie A (2010) Crops that feed the World 1. Yams. Food Security 2:305–315. https://doi.org/10.1007/s12571-010-0085-0
Burkill IH (1960) The organography and the evolution of the Dioscoreaceae, the family of the yams. Bot J Linn Soc 56:319–412. https://doi.org/10.1111/j.1095-8339.1960.tb02508.x
Caddick LR, Rudal PJ, Wilkin P (2000) Floral morphology and development in Dioscoreales. Feddes Repert 111:189–230. https://doi.org/10.1002/fedr.20001110313
Chung DH, Chung GY (2015) A taxonomic study of the genus Dioscorea L. (Dioscoreaceae) in Korea based on morphological characters. Korean J Pl Taxon 45:380–390. https://doi.org/10.11110/kjpt.2015.45.4.380
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Couto RS, Martins AC, Bolson M, Lopes RC, Smidt EC, Braga JMA (2018) Time calibrated tree of Dioscorea (Dioscoreaceae) indicates four origins of yams in the Neotropics since the Eocene. Bot J Linn Soc 188:144–160. https://doi.org/10.1093/botlinnean/boy052
Davis GL (1966) Systematic embryology of angiosperms. John Wiley and Sons, New York
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Gao X, Zhu YP, Wu BC, Zhao YM, Chen JQ, Hang YY (2008) Phylogeny of Dioscorea sect. Stenophora based on chloroplast matK, rbcL and trnL-F sequences. J Syst Evol 46:315–321. https://doi.org/10.3724/SP.J.1002.2008.08007
Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: program-oriented format conversion of DNA and protein alignments. Nucl Acids Res 38:W14–W18. https://doi.org/10.1093/nar/gkq321
Guignard JL (1963) Embriogenie des Dioscoreacees. Developpement de l’embryon chez le Tamus communis L. Compt Rend Acad Sci 256:3172–3175
Hsu KM, Tsai JL, Chen MY, Ku HM, Liu SC (2013) Molecular phylogeny of Dioscorea (Dioscoreaceae) in East and Southeast Asia. Blumea 58:21–27. https://doi.org/10.3767/000651913X669022
Huber H (1998) Dioscoreaceae. In: Kubitzki K (ed) Families and genera of vascular plants vol. 3 Flowering plants. Monocotyledons. Lilianae (except Orchidaceae). Springer Berlin Heidelberg, Berlin, pp 216–235. https://doi.org/10.1007/978-3-662-03533-7_28
Kamelina OP (2000) Embryological features in phylogenetic systematics of flowering plants. Bot Zhurn (St Petersburg) 85:22–33 (in Russian)
Kamelina OP (2009) Systematic embryology of flowering plants, vol. 1 Dycotyledons. Arctica Press, Barnaul (in Russian)
Kawabe A, Miyashita NT, Terauchi R (1997) Phylogenetic relationship among the section Stenophora in the genus Dioscorea based on the analysis of nucleotide sequence variation in the phosphoglucose isomerase (Pgi) locus. Genes Genet Systems 72:253–262. https://doi.org/10.1266/ggs.72.253
Knuth R (1924) Dioscoreaceae. In: Engler A (ed) Das Pflanzenreich. Verlag von Wilhelm Engelmann, Leipzig, pp 1–386
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molec Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Liu XT, Wang ZZ, Xiao W, Zhao HW, Hu J, Yu B (2008) Cholestane and spirostane glycosides from the rhizomes of Dioscorea septemloba. Phytochemistry 69:1411–1418. https://doi.org/10.1016/j.phytochem.2007.12.014
Maurin O, Muasya AM, Catalan P, Shongwe EZ, Viruel J, Wilkin P, Van der Bank M (2016) Diversification into novel habitats in the Africa clade of Dioscorea (Dioscoreaceae): erect habit and elephant’s foot tubers. BMC Evol Biol 16:238. https://doi.org/10.1186/s12862-016-0812-z
Noda H, Yamashita J, Fuse S, Pooma R, Poopath M, Tobe H, Tamura MN (2020a) A large-scale phylogenetic analysis of Dioscorea (Dioscoreaceae), with reference to character evolution and subgeneric recognition. Acta Phytotax Geobot 71:103–128. https://doi.org/10.18942/apg.201923
Noda H, Fuse S, Yamashita J, Pooma R, Poopath M, Tobe H, Tamura MN (2020b) A revised infrageneric classification of Old World species of Dioscorea (Dioscoreaceae). Acta Phytotax Geobot 71:187–199. https://doi.org/10.18942/apg.202003
Poddubnaya-Arnoldi VA (1976) Cytoembryology of angiosperms. Basis and perspectives. Nauka, Moscow (in Russian)
Prain D, Burkill IH (1936) An account of the genus Dioscorea in the East. Part 1: The species which twine to the left. Ann Roy Bot Gard, (Calcutta) 14:1–210
Price EJ, Wilkin P, Sarasan V, Fraser PD (2016) Metabolite profiling of Dioscorea (yam) species reveals underutilized biodiversity and renewable sources for high-value compounds. Sci Rep 6:29136. https://doi.org/10.1038/srep29136
Rao NA (1953) Embryology of Dioscorea oppositifilia L. Phytomorphology 3:121–126
Remizowa MV, Sokoloff DD, Kondo K (2010) Early flower and inflorescence development in Dioscorea tokoro Makino (Dioscoreales): shoot chirality, handedness of cincinni and common tepal-stamen primordia. Wulfenia 17:77–97
Santos AM, Cabezas MP, Tavares AI, Xavier R, Branco M (2016) tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics 32:627–628. https://doi.org/10.1093/bioinformatics/btv636
Schols P, Furness CA, Wilkin P, Smets E, Cielen V, Huysmans S (2003) Pollen morphology of Dioscorea (Dioscoreaceae) and its relation to systematics. Bot J Linn Soc 43:375–390. https://doi.org/10.1111/j.1095-8339.2003.00227.x
Schols P, Wilkin P, Furness CA, Huysmans S, Smets E (2005) Pollen evolution in yams (Dioscorea: Dioscoreaceae). Syst Bot 30:750–758
Shah HJ, Lele SS (2012) In vitro propagation of Dioscorea alata var. purpurae. Appl Biochem Biotechnol 167:1811–1817. https://doi.org/10.1007/s12010-012-9658-z
Takeuchi Y (1971) Embryo sac development in Dioscorea izuensis Akahori. Sci Rep Tohoku Univ, Ser 4, Biol 35:225–229
Takeuchi Y (1972) Embryo sac development in Dioscorea japonica Thunb. and D. quinqueloba Thunb. Acta Phytotax Geobot 25:57–60
Takeuchi Y, Kimura C (1968) On the embryo sac formation of Dioscorea nipponica Makino and D. tokoro Makino. Sci Rep Univ Tohoku, Ser 4, Biol 34:137–140
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molec Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Terui K, Kanazawa T, Yoshida M, Sasaki R, Igarashi K, Taneichi Y, Nishino E, Ding Z (2003) A rediscovery of androdioecy and pollen formation in the hermaphrodite flower in Nagaimo (Dioscorea opposita Thunb.). J Jap Bot 78:183–190
Thapyai C, Wilkin P, Chayamarit K (2005) The rediscovery of Dioscorea rockii Prain & Burkill, endemic to northern Thailand. Thai Forest Bull Bot 33:220–227
Titova GE, Torshilova AA (2015) To the evolution of seed morphological type in the Dioscorea section Stenophora (Dioscoreaceae). Bot Zhurn (St Petersburg) 100:761–786. https://doi.org/10.1134/s0006813615080013 (in Russian)
Torshilova AA, Titova GE (2010) Seed formation and morphogenetic correlations in its structures development in Dioscorea nipponica (Dioscoreaceae). Bot Zhurn (St Petersburg) 95:298–325 (in Russian)
Torshilova AA, Titova GE, Batygina TB (2003) Female reproductive structures and seed development in Dioscorea nipponica Makino (Dioscoreaceae). Acta Biol Cracov Ser Bot 45:149–154
Torshilova AA, Rudskiy IV, Shamrov II (2012) To interpretation of early stages of ovule development in Dioscorea caucasica (Dioscoreaceae). Bot Zhurn (St Petersburg) 97:734–743 (in Russian)
Torshilova AA, Vinogradova GY, Titova GE (2016) Ovule and embryo sac development in Dioscorea caucasica (Dioscoreaceae). Bot Zhurn (St Petersburg) 101:359–377. https://doi.org/10.1134/s0006813616040037 (in Russian)
Torshilova AA, Vinogradova GYu, Titova GE (2017) Development of female gametophyte in Dioscorea caucasica (Dioscoreaceae). Int J Pl Reprod Biol 9:148–152
Uline EB (1898) Eine monographie der Dioscoreaceen. Bot Jahrb Syst 25:126–165
Viruel J, Segarra-Moragues JG, Raz L, Forest F, Wilkin P, Sanmartín I, Catalán P (2016) Late Cretaceous-Early Eocene origin of yams (Dioscorea, Dioscoreaceae) in the Laurasian Palaearctic and their subsequent Oligocene-Miocene diversification. J Biogeogr 43:750–762. https://doi.org/10.1111/jbi.12678
Viruel J, Forest F, Paun O, Chase MW, Devey D, Couto RS, Segarra-Moragues JG, Catalán P, Wilkin P (2018) A nuclear Xdh phylogenetic analysis of yams (Dioscorea: Dioscoreaceae) congruent with plastid trees reveals a new Neotropical lineage. Bot J Linn Soc 187:232–246. https://doi.org/10.1093/botlinnean/boy013
Wilkin P, Schols P, Chase MW, Chayamarit K, Furness CA, Huysmans S, Rakotonasolo F, Smets E, Thapyai C (2005) A plastid gene phylogeny of the yam genus, Dioscorea: Roots, fruits and Madagascar. Syst Bot 30:736–749. https://doi.org/10.1600/036364405775097879
Zhai C, Lu Q, Chen X, Peng Y, Chen L, Du S (2009) Molecularly imprinted layer-coated silica nanoparticles toward highly selective separation of active diosgenin from Dioscorea nipponica Makino. J Chromatogr 1216:2254–2262. https://doi.org/10.1016/j.chroma.2009.01.030
Zhao Z, Wang X, Yu Y, Yuan S, Jiang D, Zhang Y, Zhang T, Zhong W, Yuan Q, Huang L (2018) Complete chloroplast genome sequences of Dioscorea: Characterization, genomic resources, and phylogenetic analyses. Peer J 6:e6032. https://doi.org/10.7717/peerj.6032
Zhinkina NA, Torshilova AA, Ozerov IO (2018) Application of modified technique of stainnig tissues of recent and fossil plants. Bot Zhurn (St Petersburg) 103:1191–1195. https://doi.org/10.7868/S0006813618090090 (in Russian)
Acknowledgements
This study was carried out within the framework of the state assignments No. AAAA-A18-118051590112-8 and AAAA-A18-118040290161-3 to Komarov Botanical Institute of the Russian Academy of Sciences (Saint Petersburg). The authors thank I.V. Tatanov, Scientific Researcher of Herbarium Department of the Komarov Botanical Institute for his advices on the Dioscorea taxonomy. The research was done using equipment of The Core Facilities Center «Cell and Molecular Technologies in Plant Science» at the Komarov Botanical Institute RAS (St. Petersburg, Russia).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling editor: Mike Thiv.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. GenBank accession numbers of specimens used in the study.
Online Resource 2. The alignment of the trnL refion of the cpDNA.
Online Resource 3. Comparison of matK and trnL networks of the section Stenophora.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Vinogradova, G., Torshilova, A. & Machs, E. Flower morphology and phylogenetic analysis of some Dioscorea species of the section Stenophora (Dioscoreaceae). Plant Syst Evol 308, 42 (2022). https://doi.org/10.1007/s00606-022-01834-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-022-01834-y