Micromorphological differentiation of Korean Disporum species using light and scanning electron microscopy
Hyeonjin Kim
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Search for more papers by this authorBokyung Choi
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Search for more papers by this authorChangyoung Lee
International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea
Search for more papers by this authorScott A. M. McAdam
Department of Botany and Plant Pathology, Purdue Center for Plant Biology, Purdue University, West Lafayette, Indiana, USA
Search for more papers by this authorJin-Hyub Paik
International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea
Search for more papers by this authorCorresponding Author
Tae-Soo Jang
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Correspondence
Tae-Soo Jang, Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon 34134, Republic of Korea.
Email: [email protected]
Search for more papers by this authorHyeonjin Kim
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Search for more papers by this authorBokyung Choi
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Search for more papers by this authorChangyoung Lee
International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea
Search for more papers by this authorScott A. M. McAdam
Department of Botany and Plant Pathology, Purdue Center for Plant Biology, Purdue University, West Lafayette, Indiana, USA
Search for more papers by this authorJin-Hyub Paik
International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea
Search for more papers by this authorCorresponding Author
Tae-Soo Jang
Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon, Republic of Korea
Correspondence
Tae-Soo Jang, Department of Biological Science, College of Bioscience and Biotechnology, Chungnam National University, Daejeon 34134, Republic of Korea.
Email: [email protected]
Search for more papers by this authorReview Editor: Paul Verkade
Abstract
The genus Disporum Salisb. is widely distributed in East Asia, yet phylogenetically relevant morphological traits useful for differentiating many of the small, perennial, herbaceous species remain poorly described. To address this, leaf, floral, pollen, and orbicule micromorphology of four Korean Disporum species was investigated using light and scanning electron microscopy. All Korean Disporum species examined had hypostomatic leaves, with anomocytic stomatal complexes found only on the abaxial epidermis. Guard cell length varied among species, ranging from 44.30 μm in D. viridescens to 53.49 μm in D. uniflorum. The epidermal cells of the investigated Disporum taxa had sinuate anticlinal cell walls on both adaxial and abaxial surfaces. The surface of the guard and subsidiary cells were either smooth with weak striations or had strongly wrinkled striations. The pollen grains of all Korean Disporum taxa were monads, monosulcate with granular aperture membranes, subprolate to prolate in shape with microreticulate or verrucate exine surfaces. The mean size of pollen grains ranged from 46.38 to 49.92 μm in polar length and from 34.39 to 39.58 μm in equatorial diameter across species. Sexine ornamentation was a taxonomically relevant trait for differentiating Korean Disporum taxa. Additionally, the presence of orbicules as well as the orbicular characters (e.g., size, shape, ornamentation, and association pattern) are described for the first time in species from this genus. The present investigation of leaf and floral micromorphology using light and scanning electron microscopy provides valuable information for the taxonomic differentiation and identification of Disporum species in Korea.
Research Highlights
- A detailed micromorphological description of leaf, floral characters (tepal, stigma, style), pollen and orbicule is provided for Korean Disporum species using scanning electron microscopy (SEM) and light microscopy (LM).
- The presence of orbicules and their taxonomic implications in Korean Disporum species are described for the first time.
- Phylogenetically informative pollen and orbicule micromorphological characters are described, improving understanding the systematic relationships of Korean species in the genus Disproum.
CONFLICT OF INTEREST
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data in this study are all provided in the figures and the part of results. Any more requests about the original data are available from the corresponding author.
REFERENCES
- Ali, M., Bahadur, S., Hussain, A., Saeed, S., Khuram, I., Ullah, M., … Akhtar, N. (2020). Foliar epidermal micromorphology and its taxonomic significance in Polygonatum (Asparagaceae) using scanning electron microscopy. Microscopy Research and Technique, 83(11), 1381–1390.
- Bahadur, S., Ahmad, M., Zafar, M., Sultana, S., Begum, N., Ashfaq, S., … Ayaz, A. (2019). Palyno-anatomical studies of monocot taxa and its taxonomic implications using light and scanning electron microscopy. Microscopy Research and Technique, 82(4), 373–393.
- Barone Lumaga, M. R., Pellegrino, G., Bellusci, F., Perrotta, E., Perrotta, I., & Musacchio, A. (2012). Comparative floral micromorphology in four sympatric species of Serapias (Orchidaceae). Botanical Journal of the Linnean Society, 169, 714–724.
- Bucher, S. F., Auerswald, K., Grün-Wenzel, C., Higgins, S. I., Jorge, J. G., & Römermann, C. (2017). Stomatal traits relate to habitat preferences of herbaceous species in a temperate climate. Flora-Morphology, Distribution, Functional Ecology of Plants, 229, 107–115.
10.1016/j.flora.2017.02.011 Google Scholar
- Byng, J. W., Chase, M. W., Christenhusz, M. J., Fay, M. F., Judd, W. S., Mabberley, D. J., … Stevens, P. F. (2016). An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1–20.
- Carrijo, T. T., Garbin, M. L., Picanço-Leite, W., Mendonça, C. B. F., Esteves, R. L., & Gonçalves-Esteves, V. (2013). Pollen morphology of some related genera of Vernonieae (Asteraceae) and its taxonomic significance. Plant Systematics and Evolution, 299, 1275–1283.
- Chao, C.-T., & Tseng, Y.-H. (2019). Taxonomic revision of Disporum Salisb. (Colchicaceae, Uvularioideae) of Taiwan. Phytokeys, 119, 1–22.
- Chen, X. Q., Liang, S. Y., Xui, J. M., & Tamura, M. N. (2000). Liliaceae. In Z.-Y. Wu & P. H. Raven (Eds.), Flora of China 24 (pp. 73–263). Beijing & Missouri Botanical Garden Press, St. Louis: Science Press.
- Chimona, C., Koukos, D., Meletiou-Christou, M.-S., Spanakis, E., Argiropoulos, A., & Rhizopoulou, S. (2018). Functional traits of floral and leaf surfaces of the early spring flowering Asphodelus ramosus in the Mediterranean region. Flora, 248, 10–21.
- Choi, B., Kim, S.-Y., & Jang, T.-S. (2020). Micromorphological and cytological comparisons between Youngia japonica and Youngia longiflora using light and scanning electron microscopy. Microscopy Research and Technique, 83(12), 1456–1463.
- Choi, B., Weiss-Schneeweiss, H., Temsch, E. M., So, S., Myeong, H.-H., & Jang, T.-S. (2020). Genome size and chromosome number evolution in Korean Iris L. species (Iridaceae Juss.). Plants, 9, 1284.
- Costa, V. B. S., Pimentel, R. M. M., Chagas, M. G. S., Alves, G. D., & Castro, C. C. (2017). Petal micromorphology and its relationship to pollination. Plant Biology, 19, 115–122.
- Demissew, S., & Harley, M. M. (1992). Trichome, seed surface and pollen characters in Stachys (Labiatae) in tropical Africa. In R. M. Harley & T. Reynolds (Eds.), Advances in Labiatate Science (pp. 149–166). UK: Kew, Royal Botanic Gardens.
- Erdtman, G. (1960). The acetolysis method: A revised description. Svensk Botanisk Tidskrift, 54, 561–564.
- Gotelli, M. M., Galati, B. G., & Zarlavsky, G. (2016). Pollen development and anther morphology in 14 species of Rhamnaceae. Plant Systematics and Evolution, 302, 1433–1444.
- Gul, S., Ahmad, M., Zafar, M., Bahadur, S., Celep, F., Sultana, S., … Ayaz, A. (2019). Taxonomic significance of foliar epidermal morphology in Lamiaceae from Pakistan. Microscopy Research and Technique, 82(9), 1507–1528.
- Hara, H. (1988). A revision of the Asiatic species of the genus Disporum (Liliaceae). The University Museum, the University of Tokyo, Bulletin, 31, 163–209.
- Hareesh, V. S., Floden, A., & Sabu, M. (2018). Disporum mishmiensis (Colchicaceae), a new species from north East India. Blumea, 63(2), 121–124.
- Hu, R.-C., Xu, W.-B., & Huang, Y.-F. (2016). Disporum sinovietnamicum sp. nov. (Colchicaceae) from South-Western Guangxi, China. Nordic Journal of Botany, 34(2), 152–155.
- Hu, Z., Zhao, Y., Zhao, C., & Liu, J. (2020). Taxonomic importance of pollen morphology in Veratrum L. (Melanthiaceae) using microscopic techniques. Microscopy Research and Technique, 83(8), 865–876.
- Huysmans, S., El-Ghazaly, G., & Smets, E. (1998). Orbicules in angiosperms: Morphology, function, distribution, and relation with tapetum types. The Botanical Review, 64(3), 240–272.
- Huysmans, S., Verstraete, B., Smets, E., & Chatrou, L. W. (2010). Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms. Plant Ecology and Evolution, 143(2), 199–211.
- Jang, T.-S., Lee, J., & Hong, S.-P. (2014). A systematic study of Glechoma L. (Lamiaceae) based on micromorphological characters and nuclear ribosomal ITS sequences. Korean Journal of Plant Taxonomy, 44(1), 22–32.
10.11110/kjpt.2014.44.1.22 Google Scholar
- Jang, T.-S., Moon, H.-K., & Hong, S.-P. (2015). Sex expression, population structure, and floral dimorphism in a gynodioecious herb, Agastache rugosa (Lamiaceae) in Korea. Flora, 215, 23–32.
- Janssens, S., Lens, F., Dressler, S., Geuten, K., Smets, E., & Vinckier, S. (2005). Palynological variation in balsaminoid Ericales. II. Balsaminaceae, Tetrameristaceae, Pellicieraceae and general conclusions. Annals of Botany, 96(6), 1061–1073.
- Klimko, M., Nowińska, R., Wilkin, P., & Wiland-Szymańska, J. (2018). Comparative leaf micromorphology and anatomy of the dragon tree group of Dracaena (Asparagaceae) and their taxonomic implications. Plant Systematics and Evolution, 304, 1041–1055.
- Kong, M.-J., & Hong, S.-P. (2019). Leaf micromorphology of the Persicaria sect. Cephalophilon (Polygonaceae) and its systematic re-evaluation. Phytotaxa, 391(3), 167–184.
- Lee, N. S. (1979). A taxonomic study of the genus Disporum in Korea. Korean Journal of Plant Taxonomy, 9(1), 67–87 (in Korean).
10.11110/kjpt.1979.9.1.067 Google Scholar
- Lee, N. S. (2007). Disporum Salisb. ex D. Don. In C. Park (Ed.), The Genera of Vascular Plants of Korea (pp. 1309–1310). Seoul: Academy Publishing Co.
- Lee, N. S., & Yeau, S. H. (1990). A palynological study on Streptopus ovalis (Ohwi) Wang et Y.C.Tang and the relative species (tribe Polygonateae, Liliaceae). Korean Journal of Plant Taxonomy, 20(2), 81–94 (in Korean).
10.11110/kjpt.1990.20.2.081 Google Scholar
- Li, X.-Z., Zhang, D.-M., & Hong, D.-Y. (2007). Disporum jinfoshanense, a new species of the Liliaceae from Chongqing, China. Acta Phytotaxonomica Sinica, 45(4), 583–586.
10.1360/aps06079 Google Scholar
- Magauer, M., Schönswetter, P., Jang, T.-S., & Frajman, B. (2014). Disentangling relationships within the disjunctly distributed Alyssum ovirense/A. wulfenianum group (Brassicaceae), including description of a novel species from the North-Eastern Alps. Botanical Journal of the Linnean Society, 176(4), 486–505.
- Membrives, N., Pedrola-Monfort, J., & Caujapé-Castells, J. (2003). Morphological seed studies of southwest African Androcymbium (Colchicaceae). Botanical Macaronésica, 24, 87–106.
- Meng, Y., Wang, J.-J., & Nie, Z.-L. (2016). Comparative morphology of leaf epidermis in 34 species of Maianthemum (Asparagaceae, Polygonateae) and their systematic significance. Phytotaxa, 275, 81–96.
- Moon, H.-K. (2018). The phylogenetic potential of orbicules in angiosperms. Korean Journal of Plant Taxonomy, 48(1), 9–23.
10.11110/kjpt.2018.48.1.9 Google Scholar
- Moon, H.-K., Vinckier, S., Smets, E., & Huysmans, S. (2008). Comparative pollen morphology and ultrastructure of Mentheae subtribe Nepetinae (Lamiaceae). Review of Paleobotany and Palynology, 149(3–4), 174–186.
- Moon, H.-K., Hong, S.-P., Smets, E., & Huysmans, S. (2009). Phylogenetic significance of leaf micromorphology and anatomy in the tribe Mentheae (Nepetoideae: Lamiaceae). Botanical Journal of the Linnean Society, 160(2), 211–231.
- Nilsson, S., & Robyns, A. (1974). Pollen morphology and taxonomy of the genus Quaraibea s.l. (Bombacaceae). Bulletin du Jardin Botanique National de Belgique, 44, 77–99.
10.2307/3667429 Google Scholar
- Park, I., Yang, S., Song, J.-H., & Moon, B. C. (2020). Dissection for floral micromorphology and plastid genome of valuable medicinal borages Arnebia and Lithospermum (Boraginaceae). Frontiers in Plant Science, 11, 606463.
- Piwowarczyk, R., & Kasińska, J. (2017). Petal epidermal micromorphology in holoparasitic Orobanchaceae and its significance for systematics and pollination ecology. Australian Systematic Botany, 30, 48–63.
- Punt, W., Hoen, P. P., Blackmore, S., Nilsson, S., & le Thomas, A. (2007). Glossary of pollen and spore terminology. Review of Paleobotany and Palynology, 143(1–2), 1–81.
- Roguz, K., Bajguz, A., Gołębiewska, A., Chmur, M., Hill, L., Kalinowki, P., … Zych, M. (2018). Functional diversity of nectary structure and nectar composition in the genus Fritillaria (Liliaceae). Frontiers in Plant Science, 9, 1246.
- Ruggiero, F., & Bedini, G. (2020). Phylogenetic and morphologic survey of orbicules in angiosperms. Taxon, 69(3), 543–566.
- Schols, P., Furness, C. A., Wilkin, P., Huysmans, S., & Smets, E. (2001). Morphology of pollen and orbicules in some Dioscorea species and its systematic implications. Botanical Journal of the Linnean Society, 136(3), 295–311.
- Shinwari, Z. K., Terauchi, R., & Kawano, S. (1994). Molecular systematics of Liliaceae-Asparagoideae-Polygonatae I. RFLP analysis of cpDNA in several Asiatic Disporum species. Plant Species Biology, 9(1), 11–18.
10.1111/j.1442-1984.1994.tb00076.x Google Scholar
- Shinwari, Z. K., Kato, H., Terauchi, R., & Kawano, S. (1994). Phylogenetic relationships among genera in the Liliaceae-Asparagoideae-Polygonatae s.l. inferred from rbcL gene sequence data. Plant Systematics and Evolution, 192, 263–277.
- Shinwari, Z. K., Terauchi, R., Utech, F. H., & Kawano, S. (1994). Recognition of the New World Disporum section Prosartes as Prosartes (Liliaceae) based on the sequence data of rbcL gene. Taxon, 43(3), 353–366.
- Song, J.-H., Moon, H.-K., Oak, M.-K., & Hong, S.-P. (2017). Phylogenetic evaluation of pollen and orbicule morphology in Rosaceae tribe Neillieae (subfamily Amygdaloideae). Botanical Journal of the Linnean Society, 183(3), 439–453.
- Stolar, J., & Davis, A. R. (2010). Floral nectary structure, nectar production, and carbohydrate composition in the Lilium Asiatic hybrid 'Trésor'. Botany, 88, 185–205.
- Takahashi, M., & Sohma, K. (1979). Pollen wall formation and tapetum in Disporum smilacinum A. Gray (Liliaceae). Science Reports of Tohoku University. 4th series (Biology), 37, 273–281.
- Tamura, M. N., Utech, F. H., & Kawano, S. (1992). Biosystematic studies in Disporum (Liliaceae-Polynogateae) IV. Karyotype analysis of some Asiatic and North American taxa with special reference to their systematic status. Plant Species Biology, 7(2–3), 103–120.
10.1111/j.1442-1984.1992.tb00224.x Google Scholar
- Tamura, M. N., Yamada, M., Fuse, S., & Hotta, M. (2013). Molecular phylogeny and taxonomy of the genus Disporum (Colchicaceae). Acta Phytotaxonomica Geobotanica, 64(3), 137–147.
- Tomaszewski, D., & Zieliński, J. (2014). Epicuticular wax structures on stems and comparison between stems and leaves: A survey. Flora-Morphology, Distribution, Functional Ecology of Plants, 209(5–6), 215–232.
10.1016/j.flora.2014.03.001 Google Scholar
- Tuler, A. C., da Silva, T., Carrijo, T. T., Garbin, M. L., Mendonça, C. B. F., Peixoto, A. L., & Gonçalves-Esteves, V. (2017). Taxonomic significance of pollen morphology for species delimitation in Psidium (Myrtaceae). Plant Systematics and Evolution, 303, 317–327.
- Verstraete, B., Groeninckx, I., Smets, E., & Huysmans, S. (2011). Phylogenetic signal of orbicules at family level: Rubiaceae as case study. Taxon, 60(3), 742–757.
- Verstraete, B., Moon, H.-K., Smets, E., & Huysmans, S. (2014). Orbicules in flowering plants: A phylogenetic perspective on their form and function. The Botanical Review, 80, 107–134.
- Vinckier, S., & Smets, E. (2002). Morphological and ultrastructural diversity of orbicules in relation to evolutionary tendencies in Apocynaceae s.l. Annals of Botany, 90(5), 647–662.
- Vinckier, S., & Smets, E. (2003). Morphological and ultrastructural diversity of orbicules in Gentianaceae. Annals of Botany, 92(5), 657–672.
- Vinckier, S., Huysmans, S., & Smets, E. (2000). Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae). Review of Paleobotany and Palynology, 108(3–4), 151–174.
- Wang, L., Gu, L., Zhao, C., & Liu, J. (2018). Pollen morphology of Polygonatae and its systematic significance. Palynology, 42(2), 255–272.
- Xiong, X.-H., Zhou, X.-M., Li, M., Xu, B., Deng, H.-N., Yu, Q., & Gao, X.-F. (2019). Pollen morphology in Rubus (Rosaceae) and its taxonomic implications. Plant Systematics and Evolution, 305, 705–716.
- Zhu, X., Liao, S., & Yi, S. (2019). Disproum nanchuanense (Colchicaceae), a new species from Chongqing, China. Phytokeys, 130, 49–57.
- Zhu, X.-X., Zhang, C., Shen, B., Liu, D.-T., & Zhang, L. (2016). Disporum xilingense (Colchicaceae), a new species from Sichuan, China, and the exclusion of D. leucanthum from the Chinese flora. Phytotaxa, 252(1), 63–68.