Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea

doi:10.1016/j.pld.2021.06.004

Plant Diversity ›› 2022, Vol. 44 ›› Issue (02): 170-180.DOI: 10.1016/j.pld.2021.06.004

• Articles • Previous Articles Next Articles

Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea

Changkyun Kim^a, Dong-Kap Kim^b, Hang Sun^c, Joo-Hwan Kim^d

a Plant Research Division, Honam National Institute of Biological Resources, Mokpo 58762, Republic of Korea;
b Forest Biodiversity Division, Korea National Arboretum, Pocheon 11186, Republic of Korea;
c CAS Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, Yunnan, PR China;
d Department of Life Science, Gachon University, Seongnam 13120, Republic of Korea

Received:2021-01-24 Revised:2021-06-03 Online:2022-04-24 Published:2022-04-25
Contact: Joo-Hwan Kim,E-mail:kimjh2009@gachon.ac.kr
Supported by:
The authors thank Drs. S. Kikuchi, S. Kanetani, and J. Worth (Forestry and Forest Products Research Institute) for help in collecting plant material. This work was supported by grants from the Korea National Arboretum (Grant no. KNA1-1-13,14-1) and Gachon University (Grant no. 2018-0320) to J-H Kim.

Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea

Changkyun Kim^a, Dong-Kap Kim^b, Hang Sun^c, Joo-Hwan Kim^d

a Plant Research Division, Honam National Institute of Biological Resources, Mokpo 58762, Republic of Korea;
b Forest Biodiversity Division, Korea National Arboretum, Pocheon 11186, Republic of Korea;
c CAS Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, Yunnan, PR China;
d Department of Life Science, Gachon University, Seongnam 13120, Republic of Korea

通讯作者: Joo-Hwan Kim,E-mail:kimjh2009@gachon.ac.kr
基金资助:
The authors thank Drs. S. Kikuchi, S. Kanetani, and J. Worth (Forestry and Forest Products Research Institute) for help in collecting plant material. This work was supported by grants from the Korea National Arboretum (Grant no. KNA1-1-13,14-1) and Gachon University (Grant no. 2018-0320) to J-H Kim.

Abstract

Abstract: Endemic plants are important for understanding phylogenetic relationships, biogeographical history, and genetic variation because of their restricted distribution and their role in conserving biodiversity. Here, we investigated the phylogenetic relationships of the Korean endemic Fraxinus chiisanensis by reconstructing the molecular phylogeny of Fraxinus based on two nuclear DNA (nrITS and phantastica) and two chloroplast DNA (psbA-trnH and rpl32-trnL) regions. Within our fossil-calibrated phylogenetic framework, we also inferred the biogeographical history of F. chiisanensis. To provide a scientific basis for the conservation of F. chiisanensis, we determined the levels of genetic diversity and genetic differentiation in this species. Combining information from nuclear and chloroplast DNA sequence data, our molecular phylogenetic analyses identified F. chiisanensis as a genetically distinct unit from its sister group, Fraxinus platypoda from Japan. Our molecular dating analyses using nuclear and chloroplast DNA data sets show F. chiisanensis diverged from its sister F. platypoda in the Early or Middle Miocene and differentiated in the Late Miocene on the Korean Peninsula. Our results suggest that the divergence of F. chiisanensis was associated with the submergence of the East China Sea land bridge and enhanced monsoons in East Asia. When compared to F. platypoda, F. chiisanensis exhibits low genetic diversity within populations and high genetic differentiation among populations. These results help us to understand the evolutionary history of F. chiisanensis and to develop a conservation strategy for this species.

Key words: East China Sea land bridge, Endemic species, Fraxinus chiisanensis, Korean Peninsula, Genetic diversity, Biogeography

摘要： Endemic plants are important for understanding phylogenetic relationships, biogeographical history, and genetic variation because of their restricted distribution and their role in conserving biodiversity. Here, we investigated the phylogenetic relationships of the Korean endemic Fraxinus chiisanensis by reconstructing the molecular phylogeny of Fraxinus based on two nuclear DNA (nrITS and phantastica) and two chloroplast DNA (psbA-trnH and rpl32-trnL) regions. Within our fossil-calibrated phylogenetic framework, we also inferred the biogeographical history of F. chiisanensis. To provide a scientific basis for the conservation of F. chiisanensis, we determined the levels of genetic diversity and genetic differentiation in this species. Combining information from nuclear and chloroplast DNA sequence data, our molecular phylogenetic analyses identified F. chiisanensis as a genetically distinct unit from its sister group, Fraxinus platypoda from Japan. Our molecular dating analyses using nuclear and chloroplast DNA data sets show F. chiisanensis diverged from its sister F. platypoda in the Early or Middle Miocene and differentiated in the Late Miocene on the Korean Peninsula. Our results suggest that the divergence of F. chiisanensis was associated with the submergence of the East China Sea land bridge and enhanced monsoons in East Asia. When compared to F. platypoda, F. chiisanensis exhibits low genetic diversity within populations and high genetic differentiation among populations. These results help us to understand the evolutionary history of F. chiisanensis and to develop a conservation strategy for this species.

关键词: East China Sea land bridge, Endemic species, Fraxinus chiisanensis, Korean Peninsula, Genetic diversity, Biogeography

Changkyun Kim, Dong-Kap Kim, Hang Sun, Joo-Hwan Kim. Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea[J]. Plant Diversity, 2022, 44(02): 170-180.

References

Akaike, H., 1974. A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19, 716-723.
Arca, M., Hinsinger, D.D., Cruaud, C., et al., 2012. Deciduous trees and the application of universal DNA barcodes: a case study on the circumpolar Fraxinus. PLoS One 7, e34089.
Bai, W.-N., Liao, W.-J., Zhang, D.-Y., 2010. Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia. New Phytol. 188, 892-901.
Bandelt, H.-J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37-48.
Call, V.B., Dilcher, D.L., 1992. Investigations of angiosperms from the Eocene of southeastern north America: samaras of Fraxinus wilcoxiana Berry. Rev. Palaeobot. Palynol. 74, 249-266.
Chang, C.-S., 2007. Fraxinus L. In: Flora of Korea Editorial Committee. The genera of vascular plants of Korea. Academy Publishing Co., Seoul, pp. 854-855.
Chang, C.-S., Min, W.-K., Jeon, J.I., 2002. Species relationships of Fraxinus chiisanensis Nakai and subsect. Miliodes of sect. Fraxinus-as revealed by morphometrics and flavonoids. Kor. J. Plant Taxon. 32, 55-76 (in Korean, with English abstract).
Chen, X.-H., Xiang, K.-L., Lian, L., et al., 2020. Biogeographic diversification of Mahonia (Berberidaceae): implications for the origin and evolution of East Asian subtropical evergreen broadleaved forests. Mol. Phylogenet. Evol. 151, 106910.
Choi, K.-R., 1998. The post-glacial vegetation history of the lowland in Korean Peninsula. Kor. J. Entomol. 21, 169-174.
Chung, C.-H., Lim, H.S., Yoon, H.J., 2006. Vegetation and climate changes during the late Pleistocene to Holocene inferred from pollen record in Jinju area, South Korea. Geosci. J. 10, 423-431.
Chung, M.Y., Chung, M.G., López-Pujol, J., et al., 2014. Were the main mountain ranges in the Korean Peninsula a glacial refugium for plants? Insights from the congeneric pair Lilium cernum-Lilium amabile. Biochem. Syst. Ecol. 53, 36-45.
Chung, M.Y., López-Pujol, J., Chung, M.G., 2017. The role of the Baekdudaegan (Korean Peninsula) as a major glacial refugium for plant species: a priority for conservation. Biol. Conserv. 206, 236-248.
Chung, T.H., 1957. Korean Flora (I) Woody Plants. Shinjisa Press, Seoul (in Korean).
Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.
Ellstrand, N.C., Elam, D.R., 1993. Population genetic consequences of small population size: implications for plant conservation. Annu. Rev. Ecol. Syst. 24, 217-242.
Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin: an integrated software for population genetics data analysis. Version 3.0. Evol. Bioinf. 1, 47-50.
Farris, J.S., Kallersjo, M., Kluge, A.G., et al., 1995. Testing significance in incongruence. Cladistics 10, 315-319.
Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
Fischer, M., Husi, R., Prati, D., et al., 2000. RAPD variation among and within small and large populations of the rare clonal plant Ranunculus reptans (Ranunculaceae). Am. J. Bot. 87, 1128-1137.
Frankham, R., 1996. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 10, 1500-1508.
Frankham, R., Ballon, J.D., Briscoe, D.A., 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge.
Ge, X.-J., Hwang, C.C., Liu, Z.H., et al., 2011. Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China. BMC Genet. 12, 1.
Ha, Y.-H., Kim, C., Choi, K., et al., 2018. Molecular phylogeny and dating of Forsythieae (Oleaceae) provide insight into the Miocene history of Eurasian temperate shrubs. Front. Plant Sci. 9, 99.
Hably, L., Kvacek, Z., Manchester, S.R., 2000. Shared taxa of land plants in the Oligocene of Europe and North America in context of Holarctic phytogeography. Acta Univ. Carol. Geol. 44, 59-74.
Hinsinger, D.D., Basak, J., Gaudeul, M., et al., 2013. The phylogeny and biogeographic history of ashes (Fraxinus, Oleaceae) highlight roles of migration and vicariance in the diversification of temperate trees. PLoS One 8, e80431.
Huang, J.H., Chen, J.-H., Ying, J.-S., et al., 2011. Features and distribution patterns of Chinese endemic seed plant species. J. Syst. Evol. 49, 81-94.
Huelsenbeck, J.P., Ronquist, F., 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
Jung, S.-H., Lee, S.-J., 2009. Fossil-winged fruits of Fraxinus (Oleaceae) and Liriodendron (Magnoliaceae) from the Duho formation, Pohang basin, Korea. Acta Geol. Sin. 83, 845-852.
Katoh, K., Rozewicki, J., Yamada, K.D., 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinf. 20, 1160-1166.
Kikuchi, R., Pak, J.-H., Takahashi, H., 2010. Disjunct distribution of chloroplast DNA haplotypes in the understory perennial Veratrum album ssp. oxysepalum (Melanthiaceae) in Japan as a result of ancient introgression. New Phytol. 188, 879-891.
Kim, C., Deng, T., Wen, J., et al., 2015. Systematics, biogeography, and character evolution of Deutzia (Hydrangeaceae) inferred from nuclear and chloroplast DNA sequences. Mol. Phylogenet. Evol. 87, 91-104.
Kim, C., Kim, H.-J., Do, H.D.K., et al., 2019. Characterization of the complete chloroplast genome of Fraxinus chiisanensis (Oleaceae), an endemic to Korea. Conserv. Genet. Resour. 11, 63-66.
Kim, C., Na, H.R., Choi, H.-K., 2008a. Conservation genetics of endangered Brasenia schreberi based on RAPD and AFLP markers. J. Plant Biol. 51, 206-268.
Kim, C., Na, H.R., Choi, H.-K., 2008b. Genetic diversity and population structure of endangered Isoëtes coreana in South Korea based on RAPD analysis. Aquat. Bot. 89, 43-49.
Kim, Y.-S., Kim, H., Son, S.-W., 2016. Fraxinus Chiisanensis. The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T13188447A13189459.en e.T13188447A13189459.
Kim, Z.S., Hwang, J.W., Lee, S., et al., 2005. Genetic variation of Korean pine (Pinus koraiensis Sieb. et Zucc.) at allozyme and RAPD markers in Korea, China, and Russia. Silvae Genet. 54, 235-246.
Lee, D.-H., Lee, J.-H., Cho, W.-B., et al., 2016. The establishment history of alpine Leontopodium japonicum (Asteraceae) resembles that of warm-temperate plants on the Korean Peninsula. Plant Syst. Evol. 302, 1483-1494.
Lee, H.S., Chang, C.-S., Kim, H., et al., 2009. A preliminary population genetic study of an overlooked endemic ash, Fraxinus chiisanensis in Korea using allozyme variation. J. Kor. For. Soc. 98, 531-538.
Lee, J.-H., Lee, D.-H., Choi, B.-H., 2013. Phylogeography and genetic diversity of East Asian Neolitsea sericea (Lauraceae) based on variations in chloroplast DNA sequences. J. Plant Res. 126, 193-202.
Lee, T.B., 1980. Illustrated Flora of Korea. Hyangmun Co., Seoul (in Korean).
Li, E.X., Sun, Y., Qiu, Y.X., et al., 2008. Phylogeography of two East Asian species in Croomia (Stemonaceae) inferred from chloroplast DNA and ISSR fingerprinting variation. Mol. Phylogenet. Evol. 49, 702-714.
Liao, Y.-Y., Gichira, W.A., Wang, Q.-F., et al., 2016. Molecular phylogeography of four endemic Sagittaria species (Alismataceae) in the Sino-Japanese floristic region of East Asia. Bot. J. Linn. Soc. 180, 6-20.
López-Pujol, J., Zhang, F.-M., Sun, H.-Q., et al., 2011. Centres of plant endemism in China: places for survival or for speciation? J. Biogeogr. 38, 1267-1280.
Maddison, W.P., 1997. Gene trees in species trees. Syst. Biol. 46, 523-536.
Meilleur, B.A., Hodgkin, T., 2004. In situ conservation of crop wild relatives: status and trends. Biodivers. Conserv. 13, 663-684.
Menges, E.S., 1991. The application of minimum viable population theory to plants. In: Falk, D.A., Honsinger, K.T. (Eds.), Genetics and Conservation of Rare Plants. Oxford University Press, New York, pp. 45-61.
Millien-Parra, V., Jaeger, J.J., 1999. Island biogeography of the Japanese terrestrial mammal assemblage: an example of a relict fauna. J. Biogeogr. 26, 959-972.
Min, W.K., Jeon, J.I., Chang, C.S., 2001. A taxonomic reconsideration of Fraxinus chiisanensis (Oleaceae) in Korea. J. Kor. For. Soc. 90, 266-276 (in Korean, with English abstract).
Nakai, T., 1929. Notulæ ad plantas Japoniæ & Koreæ XXXVII, 76. The Botanical Magazine, Tokyo, pp. 439-447.
Nakhleh, L., 2010. Evolutionary phylogenetic works. In: Heath, L., Ramakrishnan, N.(Eds.), The Problem Solving Handbook for Computational Biology and Bioinformatics. Springer, New York, pp. 125-158.
Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
Nei, M., Tajima, F., 1983. Maximum likelihood estimation of the number of nucleotide substitutions from restriction site data. Genetics 105, 207-217.
Nesom, G.L., 2014. Phylogeny of Fraxinus sect. Melioides (Oleaceae): review and an alternative hypothesis. Phytoneuron 95, 1-9.
NIBR (National Institute of Biological Resources), 2012. Red Data Book of Endangered Vascular Plants in Korea. National Institute of Biological Resources Press, Inchoen.
Nie, Z.-L., Wen, J., Azuma, H., et al., 2008. Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern hemisphere inferred three nuclear data sets. Mol. Phylogenet. Evol. 48, 1027-1040.
Nylander, J.A.A., Wilgenbusch, J.C., Warren, D.L., et al., 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24, 581-583.
Ota, H., 1998. Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu archipelago, Japan, with special reference to their paleogeographical implication. Res. Popul. Ecol. 40, 189-204.
Palamarev, E., 1989. Paleobotanical evidences of the Tertiary history and origin of the Mediterranean sclerophyll dendroflora. Plant Systemat. Evol. 162, 93-107.
Pons, O., Petit, R.J., 1996. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144, 1237-1245.
Posada, D., Crandall, K.A., 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
Qi, X.-S., Yuan, N., Comes, H.P., et al., 2014. A strong ‘filter’ effect of the East China Sea land bridge for East Asia's temperate plant species: inferences from molecular phylogeography and ecological niche modelling of Platycrater arguta(Hydrangeaceae). BMC Evol. Biol. 14, 41.
Qiu, Y.-X., Qiu, Y.X., Qi, X.S., et al., 2009a. Population genetic structure, phylogeography, and demographic history of Platycrater arguta (Hydrangeaceae) endemic to East China and South Japan, inferred from chloroplast DNA sequence variation. Taxon 58, 1226-1241.
Qiu, Y.-X., Sun, Y., Zhang, X.-P., et al., 2009b. Molecular phylogeography of East Asian Kirengeshoma (Hydrangeaceae) in relation to Quaternary climate change and land bridge configurations. New Phytol. 183, 480-495.
Rambaut, A., 2014. FigTree v1.4.2: tree drawing tool in computer program and documentation distributed by the author. http://tree.bio.ed.ac.uk/software/figtree.
Rambaut, A., Drummond, A., 2014. Tracer v1.6 in Computer Program and Documentation Distributed by the Author. http://tree.bio.ed.ac.uk/software/tracer.
Ronquist, F., Teslenko, M., Van Der Mark, P., et al., 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542.
Rozas, J., Ferrer-Mata, A., Del Barrio, J.C.S., et al., 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299-3302.
Ryu, Y., Kim, I.R., Su, M.H., et al., 2019. Phylogeographical study of Camellia japonica inferred from AFLPand chloroplast DNA haplotype analyses. J. Plant Biol. 62,14-26.
Sang, T., Crawford, D.J., Stuessy, T.F., 1997. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am. J. Bot. 84, 1120-1136.
Schwartz, M.K., Luikart, G., Waples, R.S., 2006. Genetic monitoring as a promising tool for conservation and management. Trends Ecol. Evol. 22, 26-33.
Setoguchi, H., Yukawa, T., Tokuoka, T., et al., 2006. Phylogeography of the genus Cardiandra based on genetic variation in cpDNA sequences. J. Plant Res. 119, 401-405.
Shaw, J., Lickey, E.B., Schilling, E.E., et al., 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am. J. Bot. 94, 275-288.
Song, W.B., Park, H.S., Jung, H.K., 1988. Some morphological variation of Fraxinus mandshurica Rupr. Res. Rep. Inst. For. Genet. 24, 28-34 (in Korean, with English abstract).
Spicer, R.A., 2017. Tibet, the Himalaya, Asian monsoons and biodiversity - in what ways are they related. Plant Divers. 39, 233-244.
Spicer, R.A., Farnsworth, A., Su, T., 2020. Cenozoic topography, monsoons and biodiversity conservation within the Tibetan Region: an evolving story. Plant Divers. 42, 229-254.
Stamatakis, A., Hoover, P., Rougemont, J., 2008. A rapid bootstrap algorithm for the RAxML Web Servers. Syst. Biol. 57, 758-771.
Sun, Y., Moore, M.J., Yue, L., et al., 2014. Chloroplast phylogeography of the East asian Arcto-Tertiary relict Tetracentron sinense (Trochodendraceae). J. Biogeogr. 41, 1721-1732.
Swofford, D.L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, MA. Version 4.0b10.
Volis, S., Blecher, M., 2010. Quasi in situ: a bridge between ex situ and in situ conservation of plants. Biodivers. Conserv. 19, 2441-2454.
Volis, S., Blecher, M., Sapir, Y., 2009. Complex ex situ-in situ approach for conservation of endangered plant species and its application to Iris atrofusca of the Northern Negev. BioRisk 3, 137-160.
Wallander, E., 2008. Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Syst. Evol. 273, 25-49.
Wallander, E., 2013. Systematics and floral evolution in Fraxinus (Oleaceae). Belgische Dendrologie Belge 2012, 38-58.
Wang, W., Xiang, X.-G., Xiang, K.-L., et al., 2020. A dated phylogeny of Lardizabalaceae reveals an unusual long-distance dispersal across the Pacific Ocean and the rapid rise of East Asian subtropical evergreen broadleaved forests in the late Miocene. Cladistics 36, 447-457.
Wang, Z.H., Fang, J.Y., Tang, Z.Y., et al., 2011. Patterns, determinants and models of woody plant diversity in China. Proc. R. Soc. B 278, 2122-2132.
Wei, Z., Green, P.S., 1996. Fraxinus. In: Wu, Z., Raven, P.H. (Eds.), Flora of China, vol. 15. Science Press and Missouri Botanical Garden, Missouri, pp. 273-279.
Wen, J., Nie, Z.-L., Ickert-Bond, S.M., 2016. Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. J. Syst. Evol. 54, 469-490.
Wendel, J.F., Weeden, N.F., 1989. Visualization and interpretation of plant isozymes. In: Soltis, D.E., Soltis, P.S. (Eds.), Isozymes in Plant Biology. Dioscorides Press, Portland, OR, pp. 5-45.
White, T.J., Birns, T., Lee, S., et al., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp. 315-322.
Zhang, Y.-H., Volis, S., Sun, H., 2010. Chloroplast phylogeny and phylogeography of Stellera chamaejasme on the Qinghai-Tibet Plateau and in adjacent regions. Mol. Phylogenet. Evol. 57, 1162-1172.
Zheng, H., Powell, C., Rea, D.K., et al., 2004. Late Miocene and mid-Pliocene enhancement of the East Asian monsoon as viewed from the land and sea. Global Planet. Change 41, 147-155.

[1]	Mustaqeem Ahmad, Ya-Huang Luo (罗亚皇), Sonia Rathee, Robert A. Spicer, Jian Zhang (张健), Moses C. Wambulwa, Guang-Fu Zhu (朱光福), Marc W. Cadotte, Zeng-Yuan Wu (吴增源), Shujaul Mulk Khan, Debabrata Maity, De-Zhu Li (李德铢), Jie Liu (刘杰). Multifaceted plant diversity patterns across the Himalaya: Status and outlook [J]. Plant Diversity, 2025, 47(04): 529-543.
[2]	Ibrokhimjon Ergashov, Ziyoviddin Yusupov, Alireza Dolatyari, Mina Khorasani, İsmail Eker, Nazgul Turdumatova, Georgy Lazkov, Farruhbek Rasulov, Hang Sun, Tao Deng, Komiljon Tojibaev. New insights into the molecular phylogeny and biogeographical history of Allium subgenus Melanocrommyum (Amaryllidaceae) based on plastome and nuclear sequences [J]. Plant Diversity, 2025, 47(04): 561-575.
[3]	Lang Li (李朗), Bing Liu (刘冰), Yu Song (宋钰), Hong-Hu Meng (孟宏虎), Xiu-Qin Ci (慈秀芹), John G. Conran, Rogier P.J. de Kok, Pedro Luís Rodrigues de Moraes, Jun-Wei Ye (叶俊伟), Yun-Hong Tan (谭运洪), Zhi-Fang Liu (刘志芳), Marlien van der Merwe, Henk van der Werff, Yong Yang (杨永), Jens G. Rohwer, Jie Li (李捷). Global advances in phylogeny, taxonomy and biogeography of Lauraceae [J]. Plant Diversity, 2025, 47(03): 341-364.
[4]	Kai Chen, Yan-Chun Liu, Yue Huang, Xu-Kun Wu, Hai-Ying Ma, Hua Peng, De-Zhu Li, Peng-Fei Ma. Reassessing the phylogenetic relationships of Pseudosorghum and Saccharinae (Poaceae) using plastome and nuclear ribosomal sequences [J]. Plant Diversity, 2025, 47(03): 382-393.
[5]	Jianchao Liang, Zhifeng Ding, Ganwen Lie, Zhixin Zhou, Zhixiang Zhang, Huijian Hu. Climate-driven environmental filtering determines hump-shaped elevational pattern of seed plant beta diversity in the central Himalayas [J]. Plant Diversity, 2025, 47(02): 264-272.
[6]	Zengke Zhang, Wensheng Chen, Zengyan Li, Wentao Ren, Ling Mou, Junyong Zheng, Tian Zhang, Hantang Qin, Liyi Zhou, Bile Sai, Hang Ci, Yongchuan Yang, Shekhar R. Biswas, Enrong Yan. The island rule-like patterns of plant size variation in a young land-bridge archipelago: Roles of environmental circumstance and biotic competition [J]. Plant Diversity, 2025, 47(02): 300-310.
[7]	Hong Qian, Oriol Grau. Geographic patterns and ecological causes of phylogenetic structure in mosses along an elevational gradient in the central Himalaya [J]. Plant Diversity, 2025, 47(01): 98-105.
[8]	Zhiliang Yao, Xia Pan, Xin Yang, Xiaona Shao, Bin Wang, Yun Deng, Zhiming Zhang, Qiaoming Li, Luxiang Lin. Canopy structural heterogeneity drives α and β species-genetic diversity correlations in a Chinese subtropical forest [J]. Plant Diversity, 2025, 47(01): 106-114.
[9]	Wei Gu, Ting Zhang, Shui-Yin Liu, Qin Tian, Chen-Xuan Yang, Qing Lu, Xiao-Gang Fu, Heather R. Kates, Gregory W. Stull, Pamela S. Soltis, Douglas E. Soltis, Ryan A. Folk, Robert P. Guralnick, De-Zhu Li, Ting-Shuang Yi. Phylogenomics, reticulation, and biogeographical history of Elaeagnaceae [J]. Plant Diversity, 2024, 46(06): 683-697.
[10]	Yanwei Guan, Yongru Wu, Zheng Cao, Zhifeng Wu, Fangyuan Yu, Haibin Yu, Tiejun Wang. Island biogeography theory and the habitat heterogeneity jointly explain global patterns of Rhododendron diversity [J]. Plant Diversity, 2024, 46(05): 565-574.
[11]	Linjiang Ye, Robabeh Shahi Shavvon, Hailing Qi, Hongyu Wu, Pengzhen Fan, Mohammad Nasir Shalizi, Safiullah Khurram, Mamadzhanov Davletbek, Yerlan Turuspekov, Jie Liu. Population genetic insights into the conservation of common walnut (Juglans regia) in Central Asia [J]. Plant Diversity, 2024, 46(05): 600-610.
[12]	Yixian Li, Xuyao Zhao, Manli Xia, Xinzeng Wei, Hongwei Hou. Temperature is a cryptic factor shaping the geographical pattern of genetic variation in Ceratophyllum demersum across a subtropical freshwater lake [J]. Plant Diversity, 2024, 46(05): 630-639.
[13]	Yajun Wang, Hanchen Wang, Chao Ye, Zhiping Wang, Chongbo Ma, Dongliang Lin, Xiaohua Jin. Progress in systematics and biogeography of Orchidaceae [J]. Plant Diversity, 2024, 46(04): 425-434.
[14]	Hui Feng, Achyut Kumar Banerjee, Wuxia Guo, Yang Yuan, Fuyuan Duan, Wei Lun Ng, Xuming Zhao, Yuting Liu, Chunmei Li, Ying Liu, Linfeng Li, Yelin Huang. Origin and evolution of a new tetraploid mangrove species in an intertidal zone [J]. Plant Diversity, 2024, 46(04): 476-490.
[15]	Yanjun Du, Rongchen Zhang, Xinran Tang, Xinyang Wang, Lingfeng Mao, Guoke Chen, Jiangshan Lai, Keping Ma. The mid-domain effect in flowering phenology [J]. Plant Diversity, 2024, 46(04): 502-509.

Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea

Phylogenetic relationship, biogeography, and conservation genetics of endangered Fraxinus chiisanensis (Oleaceae), endemic to South Korea

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments