Phylogenetic relationships and genetic diversity of the Korean endemic Phedimus latiovalifolius (Crassulaceae) and its close relatives.
Baekdudaegan
Crassulaceae
Genetic diversity
Glacial refugium
Korean
Single nucleotide polymorphisms
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
15 Jul 2024
15 Jul 2024
Historique:
received:
31
01
2024
accepted:
27
05
2024
medline:
16
7
2024
pubmed:
16
7
2024
entrez:
15
7
2024
Statut:
epublish
Résumé
Phedimus latiovalifolius (Y.N.Lee) D.C.Son & H.J.Kim is exclusively distributed in the high mountains in the Korean Peninsula, mainly along the Baekdudaegan mountain range. Despite its morphological and distributional distinction from other Phedimus Raf. species, its taxonomic identity and phylogenetic relationship with congeneric species remain unclear. This study employs genotyping-by-sequencing-derived genome-wide single nucleotide polymorphisms to establish the monophyly of P. latiovalifolius and its relationship with closely related species. Genetic diversity and population differentiation of P. latiovalifolius are also assessed to provide baseline genetic information for future conservation and management strategies. Our phylogenetic analyses robustly demonstrate the monophyletic nature of P. latiovalifolius, with P. aizoon (L.) 't Hart identified as its closest sister lineage. There is no genetic evidence supporting a hybrid origin of P. latiovalifolius from P. aizoon involving either P. ellacombeanus (Praeger) 't Hart or P. kamtschaticus (Fisch.) 't Hart. Population genetic analyses reveal two major groups within P. latiovalifolius. A higher genetic variation is observed in P. ellacombeanus than in the congeneric species. Notably, most of the genetic variation exists within P. latiovalifolius populations. Given its distribution and the potential role of Baekdudaegan as an East Asian Pleistocene refugia, P. latiovalifolius could be considered rare and endemic, persisting in the refugium across glacial/interglacial cycles.
Identifiants
pubmed: 39009598
doi: 10.1038/s41598-024-63272-9
pii: 10.1038/s41598-024-63272-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
16255Subventions
Organisme : National Institute of Biological Resources
ID : 2020NIBR202005201
Informations de copyright
© 2024. The Author(s).
Références
Rafinesque, C.S. No. VI. Art. 5. Museum of Natural Sciences. in The American Monthly Magazine and Critical Review Vol. 1 (ed. Biglow H.) 438 (Mercein, 1817).
Thiede, J. & Eggli, U. Crassulaceae in The families and genera of vascular plants, Vol. 9. (ed. Kubitzki, K.) 83–118. (Springer, 2007), https://doi.org/10.1007/978-3-540-32219-1_12
Ohba, H., Bartholomew, B. M., Turland, N. J. & Fu, K. New combinations in Phedimus (Crassulaceae). Novon 10, 400–402 (2000).
doi: 10.2307/3392995
't Hart, H. Infrafamilial and generic classification of the Crassulaceae in Evolution and systematics of the Crassulaceae (eds. 't Hart, H. & Eggli, U.) 159–172 (Backhuys, Leiden, 1995).
Mayuzumi, S. & Ohba, H. The phylogenetic position of eastern Asian Sedoideae (Crassulaceae) inferred from chloroplast and nuclear DNA sequences. Syst. Bot. 29, 587–598 (2004).
doi: 10.1600/0363644041744329
Gontcharova, S. B., Artyukova, E. V. & Gontcharov, A. A. Phylogenetic relationships among members of the subfamily Sedeae (Crassulaceae) inferred from the ITS region sequences of nuclear rDNA. Russ. J. Genet. 42, 654–661 (2006).
doi: 10.1134/S102279540606010X
Gontcharova, S. B. & Gontcharov, A. A. Molecular phylogeny and systematics of flowering plants of the family Crassulaceae DC. Mol. Biol. 43, 794–803 (2009).
doi: 10.1134/S0026893309050112
't Hart, H. & Bleij, B. Phedimus. in Illustrated handbook of succulent plants: Crassulaceae (ed. Eggli, U.) 196–203 (Springer, 2003).
Uhl, C. H. & Moran, R. Chromosomes of Crassulaceae from Japan and South Korea. Cytologia 37, 59–81 (1972).
doi: 10.1508/cytologia.37.59
Amano, M. Biosystematic study of Sedum L. subgenus Aizoon (Crassulaceae). I. Cytological and morphological variations of Sedum aizoon L. var. floribundum Nakai. Bot. Mag. Tokyo 103, 67–85 (1990).
doi: 10.1007/BF02488412
Amano, M. & Ohba, H. Biosystematic study of Sedum L. subgenus Aizoon (Crassulaceae). II. Chromosome numbers of Japanese Sedum aizoon var. aizoon. Bot. Mag. Tokyo 105, 431–441 (1992).
doi: 10.1007/BF02497658
Chung, G. Y., Choi, M. J., Nam, B. M. & Choi, H. J. Chromosome numbers of 36 vascular plants in South Korea. J. Asia-Pac. Biodivers. 13, 504–510 (2020).
doi: 10.1016/j.japb.2020.06.009
Chung, Y. H. & Kim, J. H. A taxonomic study of Sedum section Aizoon in Korea. Korean J. Pl. Taxon. 19, 189–227 (1989).
doi: 10.11110/kjpt.1989.19.4.189
Lee, T.B. Illustrated flora of Korea. 404–408 (Hyangmunsa, 1980).
Oh, S. Y. The phytogeographical studies of family Crassulaceae in Korea. Research Rev. Kyungpook Nat. Univ. 39, 123–159 (1985).
Lee, Y. N. New taxa on Korean flora (4). Korean J. Pl. Taxon. 22, 7–11 (1992).
doi: 10.11110/kjpt.1992.22.1.007
Son, D. C., Kim, H.-J., Moon, A.-R., Jang, C.-G. & Chang, K. S. A new combination in Phedimus (Crassulaceae), with neotypification of Sedum latifovalifolium. Phytotaxa 278, 294–296 (2016).
doi: 10.11646/phytotaxa.278.3.10
Chung, M. Y., López-Pujol, J. & Chung, M. G. Is the Baekdudaegan “the Southern Appalachians of the East”? A comparison between these mountain systems, focusing on their role as glacial refugia. Korean J. Pl. Taxon. 46, 337–347 (2016).
doi: 10.11110/kjpt.2016.46.4.337
Korea Forest Service. Baek-du-daegan. To Go Beyond the Korean Peninsula and Become Northeast Asia’s Core Ecosystem. (2016).
Lee, T.B. A natural hybrid of the genus Sedum. (S. aizokamtschatica hyb. Nov.). Natural Plant 50, 5–6 (2000). (In Korean)
Fu, K.J., Ohba, H. & Gilbert, M.G. Crassulaceae in Flora of China. (eds. Wu, Z.Y. & Raven, P.H.) 202–268 (Missouri Botanical Garden Press, 2001).
Ohba, H. Crassulaceae in Flora of Japan. (eds. Iwatsuki, K., Boufford, D.E. & Ohba, H.) 139–152 (Heibonsha Ltd., 2002).
Lee, K.-B., Yoo, Y.-G. & Park, K.-R. Morphological relationships of Korean species of Sedum L. subgenus Aizoon (Crassulaceae). Korean J. Plant Tax. 33, 1–15 (2003).
doi: 10.11110/kjpt.2003.33.1.001
Yoo, Y.-G. & Park, K.-R. A test of the hybrid origin of Korean endemic Sedum latiovalifolium (Crassulaceae). Korean J. Pl. Taxon. 46, 378–391 (2016).
doi: 10.11110/kjpt.2016.46.4.378
Moon, A. R. & Jang, C. G. Taxonomic study of genus Sedum and Phedimus (Crassulaceae) in Korea based on external morphology. Korean J. Plant Tax. 33, 116–129 (2020).
Seo, H.-S., Kim, S.-H. & Kim, S.-C. Chloroplast DNA insights into the phylogenetic position and anagenetic speciation of Phedimus takesimensis (Crassulaceae) on Ulleung and Dokdo Islands. Korea. PLoS One 15, e0239734 (2020).
pubmed: 32986762
doi: 10.1371/journal.pone.0239734
Kim, Y. et al. Plastome-based backbone phylogeny of East Asian Phedimus (Subgenus Aizoon: Crassulaceae), with special emphasis on Korean endemics. Front. Plant Sci. 14, 823 (2023).
doi: 10.3389/fpls.2023.1089165
Davey, J. W. et al. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12, 499–510 (2011).
pubmed: 21681211
doi: 10.1038/nrg3012
Favre, F., Jourda, C., Besse, P. & Charron, C. Genotyping-by-Sequencing technology in plant taxonomy and phylogeny. Methods Mol. Biol. 2222, 167–178 (2021).
pubmed: 33301094
doi: 10.1007/978-1-0716-0997-2_10
De Luca, D., Del Guacchio, E., Cennamo, P., Paino, L. & Caputo, P. Genotyping-by-sequencing provides new genetic and taxonomic insights in the critical group of Centaurea tenorei. Front. Plant Sci. 14, 1130889 (2023).
pubmed: 37260938
pmcid: 10228698
doi: 10.3389/fpls.2023.1130889
Gardner, K. M. et al. Fast and cost-effective genetic mapping in apple using next-generation sequencing. G3 Genes Genomes Genet. 4, 1681–1687 (2014).
doi: 10.1534/g3.114.011023
Liu, H. et al. An evaluation of genotyping by sequencing (GBS) to map the Breviaristatum-e (ari-e) locus in cultivated barley. BMC Genom. 15, 1–1 (2014).
Bird, K. A. et al. Population structure and phylogenetic relationships in a diverse panel of Brassica rapa L. Front. Plant Sci. 8, 321 (2017).
pubmed: 28348571
pmcid: 5346582
doi: 10.3389/fpls.2017.00321
Su, C. et al. High density linkage map construction and mapping of yield trait QTLs in maize (Zea mays) using the genotyping-by-sequencing (GBS) technology. Front. Plant Sci. 8, 706 (2017).
pubmed: 28533786
pmcid: 5420586
doi: 10.3389/fpls.2017.00706
Spindel, J. et al. Bridging the genotyping gap: Using genotyping by sequencing (GBS) to add high-density SNP markers and new value to traditional bi-parental mapping and breeding populations. Theor. Appl. Genet. 126, 2699–2716 (2013).
pubmed: 23918062
doi: 10.1007/s00122-013-2166-x
Hyun, D. Y. et al. Genotyping-by-sequencing derived single nucleotide polymorphisms provide the first well-resolved phylogeny for the genus Triticum (Poaceae). Front. Plant Sci. 11, 688 (2020).
pubmed: 32625218
pmcid: 7311657
doi: 10.3389/fpls.2020.00688
Verma, S. et al. High-density linkage map construction and mapping of seed trait QTLs in chickpea (Cicer arietinum L.) using Genotyping-by-Sequencing (GBS). Sci. Rep. 5, 1–4 (2015).
doi: 10.1038/srep17512
Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).
pubmed: 19648217
pmcid: 2752134
doi: 10.1101/gr.094052.109
Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).
pubmed: 23166502
pmcid: 3499260
doi: 10.1371/journal.pgen.1002967
Chung, M. Y., López-Pujol, J., Lee, Y. M., Oh, S. H. & Chung, M. G. Clonal and genetic structure of Iris odaesanensis and Iris rossii (Iridaceae): Insights of the Baekdudaegan Mountains as a glacial refugium for boreal and temperate plants. Plant Syst. Evol. 301, 1397–1409 (2015).
doi: 10.1007/s00606-014-1168-8
Chung, M. Y., López-Pujol, J. & Chung, M. G. The role of the Baekdudaegan (Korean Peninsula) as a major glacial refugium for plant species: A priority for conservation. Biol. Conserv. 206, 236–248. https://doi.org/10.1016/j.biocon.2016.11.040 (2017).
doi: 10.1016/j.biocon.2016.11.040
Chung, M. Y. et al. Comparison of genetic variation between northern and southern populations of Lilium cernuum (Liliaceae): implications for Pleistocene refugia. PLoS One 13, e0190520. https://doi.org/10.1371/journal.pone.0190520 (2018).
doi: 10.1371/journal.pone.0190520
pubmed: 29300767
pmcid: 5754063
Chung, M. Y. et al. Patterns of genetic diversity in rare and common orchids focusing on the Korean Peninsula: Implications for conservation. Bot. Rev. 84, 1–25 (2018).
doi: 10.1007/s12229-017-9190-5
Lee, S.-J. et al. Phylogeography of the Asian lesser white-toothed shrew, Crocidura shantungensis, in East Asia: Role of the Korean Peninsula as refugium for small mammals. Genetica 146, 211–226. https://doi.org/10.1007/s10709-018-0014-2 (2018).
doi: 10.1007/s10709-018-0014-2
pubmed: 29441472
López-Pujol, J., Zhang, F.-M., Sun, H.-Q., Ying, T.-S. & Ge, S. Centres of plant endemism in China: Places for survival or for speciation?. J. Biogeogr. 38, 1267–1280 (2011).
doi: 10.1111/j.1365-2699.2011.02504.x
Qiu, Y.-X., Fu, C.-X. & Comes, H. P. Plant molecular phylogeography in China and adjacent regions: Tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Mol. Phylogenet. Evol. 59, 225–244 (2011).
pubmed: 21292014
doi: 10.1016/j.ympev.2011.01.012
Tian, H. Z. et al. Genetic diversity in the endangered terrestrial orchid Cypripedium japonicum in East Asia: Insights into population history and implications for conservation. Sci. Rep. 8, 1–13 (2018).
doi: 10.1038/s41598-018-24912-z
Sakaguchi, S. et al. Climate oscillation during the quaternary associated with landscape heterogeneity promoted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Mol. Ecol. 21, 3823–3838 (2012).
pubmed: 22646502
doi: 10.1111/j.1365-294X.2012.05652.x
Kim, Z. S., Hwang, J. W., Lee, S. W., Yang, C. & Gorovoy, P. G. 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 (2005).
doi: 10.1515/sg-2005-0034
Chen, D. et al. Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: Multiple glacial refugia and mainland-migrated island populations. PLoS One 7, e47268 (2012).
pubmed: 23115642
pmcid: 3480369
doi: 10.1371/journal.pone.0047268
Kikuchi, R., Pak, J.-H., Takahashi, H. & Maki, M. 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. https://doi.org/10.1111/j.1469-8137.2010.03398.x (2010).
doi: 10.1111/j.1469-8137.2010.03398.x
pubmed: 20659302
Hewitt, G. The genetic legacy of the quaternary ice ages. Nature 405, 907–913 (2000).
pubmed: 10879524
doi: 10.1038/35016000
Provan, J. & Bennett, K. D. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564–571 (2008).
pubmed: 18722689
doi: 10.1016/j.tree.2008.06.010
Chung, M. Y., López-Pujol, J. & Chung, M. G. Comparative genetic structure between Sedum ussuriense and S. kamtschaticum (Crassulaceae), two stonecrops co-occurring on rocky cliffs. Am. J. Bot. 101, 946–956 (2014).
pubmed: 24907251
doi: 10.3732/ajb.1400108
Hamrick, J.L. & Godt, M.J.W. Allozyme diversity in plant species in Plant Population Genetics. Breeding and Genetic Resources (eds. Brown, A.H.D., Clegg, M.T. & Weir, B.S.) 43–63 (Sinauer Associates, 1989).
Holsinger, K. E. & Weir, B. S. Genetics in geographically structured populations: Defining, estimating and interpreting F
doi: 10.1038/nrg2611
Ballesteros-Mejia, L., Lima, N. E., Lima-Ribeiro, M. S. & Collevatti, R. G. Pollination mode and mating system explain patterns in genetic differentiation in Neotropical plants. PLoS One 11, e0158660 (2016).
pubmed: 27472384
pmcid: 4966973
doi: 10.1371/journal.pone.0158660
Gibbs, R.D. Botany: An evolutionary approach. (The Blakiston Company, 1950).
Brodie, H. J. The splash-cup dispersal mechanism in plants. Can. J. Bot. 29, 224–234 (1951).
doi: 10.1139/b51-022
Nakanishi, H. Splash seed dispersal by raindrops. Ecol Res. 17, 663–671 (2002).
doi: 10.1046/j.1440-1703.2002.00524.x
Elshire, R. J. et al. A robust, simple genotyping-by sequencing (GBS) approach for high diversity species. PLoS One 6, e19379. https://doi.org/10.1371/journal.pone.0019379 (2011).
doi: 10.1371/journal.pone.0019379
pubmed: 21573248
pmcid: 3087801
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. https://doi.org/10.14806/ej.17.1.200 (2011).
doi: 10.14806/ej.17.1.200
Cox, M. P., Peterson, D. A. & Biggs, P. J. SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform. 11, 485. https://doi.org/10.1186/1471-2105-11-485 (2010).
doi: 10.1186/1471-2105-11-485
Parra-Salazar, A., Gomez, J., Lozano-Arce, D., Reyes-Herrera, P. H. & Duitama, J. Robust and efficient software for reference-free genomic diversity analysis of genotyping-by-sequencing data on diploid and polyploid species. Mol. Ecol. Resour. 22, 439–454 (2022).
pubmed: 34288487
doi: 10.1111/1755-0998.13477
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics. 27, 2156–2158 (2011).
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: An analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).
pubmed: 23701397
pmcid: 3936987
doi: 10.1111/mec.12354
Purcell, S. et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 17701901
pmcid: 1950838
doi: 10.1086/519795
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Trifinopoulos, J., Nguyen, L. T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44, W232–W235 (2016).
pubmed: 27084950
pmcid: 4987875
doi: 10.1093/nar/gkw256
Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
pubmed: 29077904
doi: 10.1093/molbev/msx281
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Kubatko, L. S. & Degnan, J. H. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56, 17–24. https://doi.org/10.1080/10635150601146041 (2007).
doi: 10.1080/10635150601146041
pubmed: 17366134
Swofford, D.L. Version 4.0a169; Phylogenetic Analysis Using Parsimony (PAUP). (2020). http://phylosolutions.com/paup-test/
Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).
pubmed: 33885785
pmcid: 8265157
doi: 10.1093/nar/gkab301
Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes - application to human mitochondrial-DNA restriction data. Genetics 131, 479–491 (1992).
pubmed: 1644282
pmcid: 1205020
doi: 10.1093/genetics/131.2.479
Meirmans, P. G. GENODIVE version 3.0: Easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol. Ecol. Resour. 20, 1126–1131 (2020).
pubmed: 32061017
pmcid: 7496249
doi: 10.1111/1755-0998.13145
Liu, X. & Fu, Y. X. Stairway Plot 2: Demographic history inference with folded SNP frequency spectra. Genome Biol. 21, 280 (2020).
pubmed: 33203475
pmcid: 7670622
doi: 10.1186/s13059-020-02196-9
You, J. et al. Comparative phylogeography study reveals introgression and incomplete lineage sorting during rapid diversification of Rhodiola. Ann. Bot. 129, 185–200 (2022).
pubmed: 34718397
doi: 10.1093/aob/mcab133
Fitak, R. R. OptM: Estimating the optimal number of migration edges on population trees using Treemix. Biol. Methods Protoc. 6, bpab017 (2021).
pubmed: 34595352
pmcid: 8476930
doi: 10.1093/biomethods/bpab017
Reich, D., Thangaraj, K., Patterson, N., Price, A. L. & Singh, L. Reconstructing Indian population history. Nature 461, 489–494 (2009).
pubmed: 19779445
pmcid: 2842210
doi: 10.1038/nature08365