1. Please check and comment entries here.
Table of Contents

    Topic review

    Clematis L. (Ranunculaceae) in Korea

    Subjects: Plant Sciences
    View times: 66
    Submitted by: Balkrishna Ghimire


    Clematis, a widely distributed genus in Ranunculaceae, is one of the most difficult groups of taxa from a taxonomic point of view. A study on achene morphology and anatomy indicated that some of the achene features could be useful as an alternative source to highlight the infrageneric relationship within the genus.  

    1. Introduction 

    Clematis L. is one of the largest genera in Ranunculaceae with about 280–350 species [1][2][3] most of which are woody or herbaceous vines, but a few are shrubs, subshrubs, or erect perennial herbs. The genus is widely distributed throughout the world but with considerable diversity in temperate and subtropical regions of the Northern Hemisphere, especially eastern Asia. China, which is believed to be the center of diversity of the genus, alone has 147 species, of which 93 are endemic [4][5][6]. Its remarkable climatic plasticity, showy flowers, and easy hybridization process make Clematis a horticulturally important genus that is widely cultivated in Europe, North America, and East Asian countries [7].

    2. Classifications

    With respect to morphology-based monographs, Clematis has been subjected to several infrageneric classifications [1][3][4][5][8][9]. Tamura [1] divided Clematis into four subgenera including 16 sections some of which were subdivided into subsections and series. Grey-Wilson [4] later grouped 297 species in nine subgenera, 16 sections, and 26 subsections whereas Johnson [5] recognized 18 sections and 36 subsections covering 325 species of the genus. Based on analyses of the various morphological and palynological characters of 345 Clematis species, Wang and Li [3] more recently purposed a system of classification establishing four subgenera two similar to those of Tamura [1] and two new subgeneric names within the genus, which are further divided into 15 sections and numerous subsections and series. These three classification systems largely agree with one another on species separations but vary in infrageneric discrimination. In this study, we follow Johnson [5][9] for infrageneric classification and Lee [10], Chang et al. [11], the Korea National Arboretum [12], and Kim [13] for species delimitations.

    According to a comprehensive classification of Ranunculaceae by Tamura [2], Clematis belongs to the tribe Anemoneae of the subfamily Ranunculoideae. Furthermore, within Anemoneae the genus has been considered to be closely related to two small genera Archiclematis (Tamura) Tamura and Naravelia DC., which are together grouped in the subtribe Clamatidinae [2]. Morphologically, these three genera share a similar climbing habit and persistent hairy style in their mature achenes. The only feature that distinguishes the monotypic genus Archiclematis within the subtribe is the alternate leaf phyllotaxy. However, the close affinity of Archiclematis alternata (Kitam. and Tamura) Tamura—including similar flower morphology—with the subgenus Viorna Gray in Clematis led Wang and Li [3], Grey-Wilson [4], Wang and Bartholomew [6], and Johnson [9] to include this species within Clematis.

    Several studies considering various morphological, anatomical, palynological, and cytological characters of Clematis have been performed [1][2][3][4][9][14][15][16][17][18][19][20][21][22][23][24][25]. Unfortunately, none of these morphological characters seem to provide enough information to resolve the infrageneric ambiguity of this large genus. As morphological and anatomical characters are subject to varied interpretations, the accurate infrageneric classification of this large genus, especially at the sectional level remains notoriously difficult. Due to this complex morphological variation within the genus and the different characters underlined in each system, the existing classifications systems for the genus diverge from one other [1][3][4][5][8][9]. Several molecular phylogenetic studies have also been performed in recent years [26][27][28][29][30][31] mostly supporting the monophyly of Clematis with clear suggestions for the retention of Archiclematis and Naravelia in a separate section within Clematis [27][29][30]. Unfortunately, the phylogenetic hypotheses supported by the morphological data were vastly incompatible with molecular hypotheses. Lehtonen et al. [31] recently studied 132 taxa of Clematis to clarify the infrageneric relationships within the genus by optimizing the phenotypic and molecular data. Their results [31] do not agree with the previous subgeneric classifications of the genus due to poor support, short branch lengths and a lack of morphologically designated units. However, they obtained 12 stable and well supported clades conceptually matching the sectional divisions of Johnson [5][9].

    Fruit and seed morphological characters have contributed useful phylogenetic data and are thus frequently used to discriminate the taxa in different taxonomic ranks. In particular, the surface sculpture of fruits, seeds or a combination of both provided a valuable reference for phylogenetic and/or systematic studies [32][33][34][35][36][37][38][39][40]. Different researchers have performed fruit and seed morphological studies emphasizing the taxonomic value of several Ranunuculaceae taxa [14][39][41][42][43][44][45][46][47][48][49][50][51][52] but studies pertaining to the fruit morphology and anatomy of Clematis are entirely absent in previous reports. Previous molecular phylogenetic studies [27][29] concluded that many morphological features in this genus traditionally considered to be useful for determining systematic relationships were highly homoplasious and not phylogenetically indicative. However, Lehtonen et al. [31] believed that the careful re-analysis of characters may facilitate a much better character coding and understanding of morphological evolution in Clematis.

    There is a longstanding argument among plant taxonomists regarding the exact number of species and taxonomic nomenclature of the Clematis taxa in Korea. Nakai [53] reported 21 species and 14 varieties of Clematis in a synoptical sketch of Korean flora but Lee [54] later described 16 species, 11 varieties, and five forma in the genus. Before Moon et al. [55], who claimed a new record of C. takedana Makino in Korea, the Korea National Arboretum and The Plant Taxonomic Society of Korea [56] included 24 taxa of Clematis in the synonymic list of vascular plants in Korea. Despite the new record of C. takedana claimed by Moon et al. [55], the origin and distribution of this species are doubtful, and not all taxonomists have accepted this taxon [10][11][12][13]. In the book New Flora of Korea, Lee [8] described 18 taxa including C. taeguensis Y. Lee, which was first described by Lee [57], whereas Chang et al. [8] only described 12 species and three varieties in the Illustrated Encyclopedia of Fauna & Flora of Korea. Clematis taeguensis was not included in the Illustrated Encyclopedia of Fauna & Flora [10] and The Flora of Korea [13] although it has been recognized as an accepted species name in the World Flora Online (WFO) [58]. The Korea National Arboretum [12] recently listed 17 species and five varieties of Clematis in the Checklist of Vascular Plants in Korea whereas Kim [13] described 13 species and seven varieties within the genus in The Flora of Korea. After a careful review of Lee [10], Chang et al. [11], the Korea National Arboretum [12], and Kim [13] we have included 16 species and three varieties, taking C. takedana as an individual species.

    3. Conclusions

    Achene indumentum, surface sculpture, and pericarp and endocarp structure proved to be the most useful achene features for characterizing Clematis taxa. The results also indicated that taxa of section Atragene and Tubulosae displayed similarity in certain key achene features; however, the number of taxa sampled was very low for these sections, and thus any interpretation made on this basis is arbitrary. Further studies considering as many taxa as possible from different sections will certainly be helpful for resolving the taxonomy of the genus. The understanding from this study is that achene morphology alone as a single source of characters, cannot be expected to elucidate the problematic infrageneric relationships but a thorough analysis of current and other morphological, as well as molecular data, will be helpful to accomplish this. Our results, however, demonstrated that achene features can contribute valuable information and could be used as descriptive and/or diagnostic characters of the Clematis species.

    This entry is adapted from 10.3390/plants9101279


    1. Tamura, M.A. Classification of genus Clematis. Acta Phytotaxon. Geobot. 1987, 38, 33–44.
    2. Tamura, M. Angiospermae: Ordnung Ranunculales. Fam. Ranunculaceae. In Die Natürlichen Pflanzenfamilien; Hiepko, P., Ed.; Duncker and Humblot: Berlin, Germany, 1995; Volume 17, pp. 324–349.
    3. Wang, W.T.; Li, L.Q. A new system of classification of the genus Clematis (Ranunculaceae). Acta Phytotaxon. Sin. 2005, 43, 431–488.
    4. Grey-Wilson, C. Clematis the Genus: A Comprehensive Guide for Gardeners, Horticulturists and Botanists; Timber Press: Portland, OR, USA, 2000.
    5. Johnson, M. The Genus Clematis; Magnus Johnson Plantskola: Stockholm, Sweden, 2001.
    6. Wang, W.T.; Bartholomew, B. Clematis . In Flora of China; Wu, Z.Y., Raven, P., Eds.; Science Press: Beijing, China; Missouri Botanical Garden Press: St. Louis, MO, USA, 2001; Volume 6.
    7. Ellitto, A.C. Systematics of Clematis in Nepal, the Evolution of Tribe Anemoneae DC. (Ranunculaceae) and Phylogeography and Dynamics of Speciation in the Himalaya. Ph.D. Thesis, University of Edinburgh, Edinburgh, UK, 2016.
    8. Prantl, K. Beitrage zur Morphologie und Systematik der Ranunculaceen. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 1888, 9, 225–273.
    9. Johnson, M. Slaktet Klematis; Magnus Johnson Plantskola: Stockholm, Sweden, 1997.
    10. Lee, Y.N. New Flora of Korea; Kyo-Hak Publishing Co. Ltd.: Seoul, Korea, 2007; Volume I.
    11. Chang, C.S.; Kim, H.; Chang, K.S. Illustrated Encyclopedia of Fauna and Flora of Korea. Woody Plants; Ministry of Education Science and Technology: Seoul, Korea, 2011; Volume 43, 511p.
    12. Chang, K.S.; Son, D.C.; Lee, D.-H.; Choi, K.; Oh, S.H. Checklist of Vascular Plants in Korea; Korea National Arboretum: Pocheon-Si, Korea, 2017; 1000p.
    13. Kim, J.S. Clematis, L. In Flora of Korea. Magnoliidae; Flora of Korea Editorial Committee and the National Institute of Biological: Gyeongsangbuk-do, Korea, 2017; Volume 2a, pp. 69–76.
    14. Tamura, M. Systema clematidis asiae orientalis. Sci. Rep. 1955, 4, 43–55.
    15. Tamura, M. Ranunculaceae. In The Families and Genera of Vascular Plants; Kubitzki, K., Rohwer, J.G., Bittrich, V., Eds.; Springer: Berlin/Heidelberg, Germany, 1993; Volume 2, pp. 563–583.
    16. Tobe, H. Morphological studies on the genus Clematis Linn. I. Pollen grains. Sci. Rep. Tohoku Univ. Fourth Ser. Biol. 1974, 37, 47–53.
    17. Tobe, H. Morphological studies on the genus Clematis Linn. V. vascular anatomy of the calyx region in four-sepaled flowers. Bot. Mag. Tokyo 1980, 93, 39–54.
    18. Tobe, H. Morphological studies on the genus Clematis Linn. VI. Vascular anatomy of the androecial and gynoecial regions of the floral receptacle. Bot. Mag. Tokyo. 1980, 93, 125–133.
    19. Tobe, H. Morphological studies on the genus Clematis Linn. VII. Reinvestigation of Clematis williamsii A. Gray and proposal of its taxonomic transfer to Clematopsis. Bot. Mag. Tokyo. 1980, 93, 135–148.
    20. Essig, F. Seedling morphology in Clematis (Ranunculaceae) and its taxonomic implications. Sida 1991, 14, 377–390.
    21. Zhang, Y.L. Chromosome studies on 7 species of Clematis in China. J. Wuhan Bot. Res. 1991, 9, 107–113.
    22. Snoeijer, W. A suggested classification for the genus Clematis. Clematis 1992, 7–20.
    23. Yano, Y. Pollen grain morphology in Clematis (Ranunculaceae). Clematis 1993, 42–43.
    24. Yang, T.Y.; Moore, D.M. A revision of the Viorna group of species (section Viorna sensu Prantl) in the genus Clematis (Ranunculaceae). Syst. Geogr. Plant. 1999, 68, 281–303.
    25. Shi, J.H.; Li, L.Q. Leaf epidermal feature in Clematis (Ranunculaceae) with reference to its systematic significance. Acta Bot. Sin. 2003, 45, 257–268.
    26. Miikeda, O.; Koga, S.; Handa, T.; Yukawa, T. Subgeneric relationships in Clematis (Ranunculaceae) by DNA sequences. In Taxonomy of Cultivated Plants: Third International Symposium; Andrews, S., Leslie, A., Alexander, C., Eds.; Royal Botanic Gardens Kew: London, UK, 1999; pp. 355–358.
    27. Miikeda, O.; Kita, K.; Handa, T.; Yukawa, T. Phylogenetic relationships of Clematis (Ranunculaceae) based on chloroplast and nuclear DNA sequences. Bot. J. Linn. Soc. 2006, 152, 153–168.
    28. Slomba, J.M.; Garey, J.R.; Essig, F.B. The actin I intron–a phylogenetically informative DNA region in Clematis (Ranunculaceae). Sida 2004, 21, 879–886.
    29. Xie, L.; Wen, J.; Li, L.Q. Phylogenetic analyses of Clematis (Ranunculaceae) based on sequences of nuclear ribosomal ITS and three plastid regions. Syst Bot. 2011, 36, 907–992.
    30. Jiang, N.; Zhou, Z.; Yang, J.B.; Zhang, S.D.; Guan, K.Y.; Tan, Y.H.; Yu, W.B. Phylogenetic reassessment of tribe Anemoneae (Ranunculaceae): Non-monophyly of Anemone s.l. revealed by plastid datasets. PLoS ONE 2017, 12, e0174792.
    31. Lehtonen, S.; Christenhusz, M.J.M.; Falck, D. Sensitive phylogenetics of Clematis and its position in Ranunculaceae. Bot. J. Linn. Soc. 2016, 182, 825–867.
    32. Fukuhara, T. Seed and funicle morphology of Fumariaceae-Fumarioideae: Systematic implications and evolutionary patterns. Int. J. Plant Sci. 1999, 160, 151–180.
    33. Juan, R.; Pastor, J.; Fernandez, I. SEM and light microscope observations on fruit and seeds in Scrophulariaceae from Southwest Spain and their systematic significance. Ann. Bot. 2000, 86, 323–338.
    34. Moro, F.V.; Pinto, A.C.R.; Dos Santos, J.M.; Filho, C.F.D. A scanning electron microscopy study of post-seminal development in Angelonia salicarii folia Bonpl. (Scrophulariaceae). Ann. Bot. 2001, 88, 499–506.
    35. Ozcan, T. SEM observations on petals and fruits of some Turkish endemic Bupleurum, L. (Umbelliferae) species. Bot. J. Linn. Soc. 2002, 138, 441–449.
    36. Xu, F. Sclerotesta morphology and its systematic implications in Magnoliaceous seeds. Bot. J. Linn. Soc. 2003, 142, 407–424.
    37. Zhang, Z.Y.; Yang, D.Z.; Lu, A.M.; Knapp, S. Seed morphology of the tribe Hyoscyameae (Solanaceae). Taxon 2005, 54, 71–83.
    38. Amini, E.; Zarre, S.; Assadi, M. Seed micro-morphology and its systematic significance in Gypsophila (Caryophyllaceae) and allied genera. Nor. J. Bot. 2011, 29, 660–669.
    39. Ghimire, B.; Jeong, M.J.; Choi, G.E.; Lee, H.; Suh, G.K.; Heo, K.; Ku, J.J. Seed morphology of the subfamily Helleboroideae (Ranunculaceae) and its systematic implication. Flora 2015, 216, 6–25.
    40. Ghimire, B.; Jeong, M.J.; Lee, K.M.; Heo, K.; Lee, C.H.; Suh, G.U. Achene morphology of Saussurea species (Asteraceae, Cardueae) in Korea and its systematic implications. Bot. J. Linn. Soc. 2016, 181, 692–710.
    41. Ghimire, B.; Lee, H.; Choi, G.E.; Jeong, M.J.; Lee, C.H.; Suh, G.U.; Heo, K.; Son, S.W. Seed morphology of 12 taxa of the genus Thalictrum, L. (Thalictroideae, Ranunculaceae) and its systematic implication. Phytotaxa 2016, 283, 271–285.
    42. Cappelletti, E.M.; Poldini, L. Seed morphology in some European aconites (Aconitum, Ranunculaceae). Plant Syst. Evol. 1984, 145, 193–201.
    43. Chaudhary, R.P.; Trifonova, V.I. Morphology of fruit and comparative anatomy of pericarp and seed coat in the Nepal species of the genus Anemone (Ranunculaceae). Bot. Z. 1988, 73, 803–817.
    44. Constantinidis, T.; Psaras, G.K.; Kamari, G. Seed morphology in relation to infrageneric classification of Consolida (DC.) Gray (Ranunculaceae). Flora 2001, 196, 81–100.
    45. Dadandi, M.Y.; Kökdil, G.; İlçim, A.; Ozbilgin, B. Seed macro and micro morphology of the selected Nigella (Ranunculaceae) taxa from Turkey and their systematic significance. Biologia 2009, 64, 261–270.
    46. Heiss, A.G.; Kropf, M.; Sontag, S.; Weber, A. Seed morphology of Nigella s.l. (Ranunculaceae): Identification, diagnostic traits, and their potential phylogenetic relevance. Int. J. Plant Sci. 2011, 172, 267–284.
    47. Ilaraslan, H.; Ilarslan, R.; Blanche, C. Seed morphology of genus Delphinium, L. (Ranunculaceae) in Turkey. Collect. Bot. 1997, 23, 79–95.
    48. Karcz, J.; Tomzcok, J. Microstructural features of seeds surface in 6 Species of the genus Nigella, L. (Ranunculaceae). Acta Biol. Siles. 1987, 7, 111–125.
    49. Luo, Y.; Zhang, F.M.; Yang, Q.E. Phylogeny of Aconitum subgenus Aconitum (Ranunculaceae) inferred from ITS sequences. Plant Syst. Evol. 2005, 252, 11–25.
    50. Wang, W.; Lu, A.M.; Ren, Y.; Endress, M.E.; Chen, Z.D. Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data. Perspect. Plant Ecol. Evol. Syst. 2009, 11, 81–110.
    51. Ziman, S.N.; Bulakh, E.V.; Kadota, Y.; Keener, C.S. Modern view on the taxonomy of the genus Anemone, L. sensu stricto (Ranunculaceae). J. Jap. Bot. 2008, 83, 127–155.
    52. Maciejewska-Rutkowska, I.; Antkowska, W. Taxonomic utility of achene morphology and anatomy in Anemone, L. (Ranunculaceae) species. Acta Biol. Carcov. Bot. 2013, 55, 29–36.
    53. Nakai, T. Synoptical sketch of the Korean Flora. Bull. Natl. Sci. Mus. 1952, 31, 1–152.
    54. Lee, C.B. Illustrated Woody Plants of Korea; Forest Experiment Station: Seoul, Korea, 1967; pp. 1–384.
    55. Moon, A.R.; Han, J.E.; Lee, B.Y.; Park, J.M.; Jang, C. An unrecorded species of genus Clematis (Ranunculaceae) from Korea. J. Asia Pac. Biodivers. 2013, 6, 415–418.
    56. Korea National Arboretum and the Plant Taxonomic Society of Korea. A Synonymic List of Vascular Plants in Korea; Korea National Arboretum: Pocheon, Korea, 2007. (In Korean)
    57. Lee, Y.N. New taxa of Korean flora (4). Korean J. Bot. 1982, 25, 175–180.
    58. World Flora Online (WFO). WFO: Clematis taeguensis Y.N.Lee. 2020. Available online: http://www.worldfloraonline.org/taxon/wfo-0000610734 (accessed on 20 August 2020).