Abstract
Pinus densiflora and Pinus thunbergii are important forest tree species in the DPR Korea due to their ecological adaptability and versatile uses, including timber, medicinal, and cosmetic production. P. thunbergii ‘Kumyahuksong’ is a significant windbreak tree species on the coast due to its high salt tolerance, pest resistance, and rapid growth. Understanding the genetic relationships of Pinus species, with the potential for natural crosses, would assist forest establishment and conservation strategies. In this study, the genetic relationship among 63 germplasms of pine species were analyzed using RAPD and ISSR markers. The populations of both species and cultivars displayed significant genetic differentiation, as evidenced by the high FST values ranging from 0.53 to 0.72. PCA and UPGMA clustering analyses revealed that the samples could be separated into major clusters according to their species. Firstly, P. densiflora and P. thunbergii were separated, followed by the separation of P. thunbergii ‘Kumyahuksong’. The Bayesian Structure analysis further emphasized the distinctiveness of P. thunbergii ‘Kumyahuksong’, particularly at K = 3, where it was presented as a distinct group. Despite the ‘Kumyahuksong’ cultivar indicated higher inbreeding (FIS = 0.261), it was also found to have a higher number of observed and effective alleles and polymorphisms compared to P. thunbergii. These results confirm the cultivar status of P. thunbergii ‘Kumyahuksong’, and also indicate that its exceptional phenotypic characteristics are likely due to its specific genetic background. Identification of natural crosses and fingerprinting of such individuals are valuable to effectively select materials in breeding programs of P. thunbergii, and the related species.
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References
Angela Rubio–Moraga, Candel–Perez D, Manuel E, Lucas–Borja PA, Tiscar B, Viñegla JC, Linares (2012) Lourdes Gómez–Gómez, Oussama Ahrazem Genetic diversity of Pinus nigra Arn. populations in southern Spain and northern Morocco revealed by inter–simple sequence repeat profiles. Int J Mol Sci 13: 5645–5658
Chapman HH (1922) A new hybrid pine (Pinus palustris × Pinus taeda). J For 20:729–734
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Dvorak WS, Jordon AP, Hodge GP, Romero JL (2000) Assessing evolutionary relationships of pines in the Oocarpae and Australes subsections using RAPD markers. New For 20:163–192
Edwards–Burke MA, Hamrick JL, Price RA (1997) Frequency and direction of hybridization in sympatric populations of Pinus taeda and P. echinata (Pinaceae). Am J Bot 84:879–886
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Goto S, Miyahara F, Ide Y (2002) Monitoring male reproductive success in a japanese black pine clonal seed orchard with RAPD markers. Can J Forest Res 32:983–988
Goudet J (2003) FSTAT (ver. 2.9.4), a program to estimate and test population genetics parameters. https://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 21 November 2003
Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Israel Jaime Ávila–Flores, José Ciro Hernández–Díaz, Maria Socorro González–Elizondo, José Ángel Prieto–Ruíz, Christian Wehenkel (2016) Degree of hybridization in seed stands of Pinus engelmannii Carr. In the Sierra Madre Occidental, Durango, Mexico, PLOS ONE, https://doi.org/10.1371/journal.pone.0152651
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a fnite population. Genetics 49:725–738
Kovacevic D, Nikolic B, Drinic SM, Bojovic S, Dodos T, Rajcevic N, Marin PD (2013) Genetic relationships among some Pinus, Picea and Abies species revealed by RAPD markers. Genetika 45(2):493–502
Labokas J, Lo žienė K, Jurevičiūtė R (2017) Preconditions for industrial use of foliage as felling by–product of Scots pine for essential oil production. Ind Crop Prod 109:542–547
Mehes MS, Nkongolo KK, Michael P (2007) Genetic analysis of Pinus strobus and Pinus monticola populations from Canada using ISSR and RAPD markers: development of genome–specific SCAR markers. Plant Syst Evol 267:47–63
Mergen F (1958) Genetic variation in needle characteristics of slash pine and in some of its hybrids. Silvae Genet 7:1–9
Mergen F, Stairs GR, Snyder EB (1965) Natural and controlled loblolly × short leaf pine hybrids in Mississippi. For Sci 11:306–314
Monteleone L, Ferrazzini D, Belletti P (2006) Effectiveness of neutral RAPD markers to detect genetic divergence between the subspecies unánata and mugo of Pinus mugo Turra. Silva Fenn 40:391–406
Naugžemys D, Žvingila D, Au čina A, Ran čelis V (2006) Comparison of DNA polymorphism in seedlings of Pinus sylvestris L. from different populations by RAPD markers. Biologijia 1:30–35
Nei M (1987) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nkongolo KK, Michael P, Gratton WS (2002) Identification and characterization of RAPD markers inferring genetic relationships among Pine species. Genome 45:51–58
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Wen X, Falush D (2009) STRUCTURE version 2.3.1 [computer program]. Available from:http://pritch.bsd.uchicago.edu/structure.html
Rohela GK, Shabnam AA, Pawan S, Ravindra A, Mudasir G, Srinvasulu Y, Sharma SP (2018) In vitro clonal propagation of PPR–1, a superior temperate mulberry variety. Indian J Biotechnol 17(4):619–625
Rohlf FJ (2008) NTSYSpc: Numerical taxonomy system, ver. 2.20. Exerter Publishing Ltd., Setauket, New York
Rosemarie Walter, Bryan K, Epperson (2005) Geographic pattern of genetic diversity in Pinus resinosa: contact zone between decendants of glacial refugia. Am J Bot 92(1):92–100
Shasany AK, Darokar MP, Dhawan S, Gupta AK, Gupta S, Shukla AK, Khanuja SP (2005) Use of RAPD and AFLP markers to identify inter–and intraspecific hybrids of Mentha. J Hered 96:542–549
Smouse PE, Saylor LC (1973) Studies of the Pinus rigida–serotina complex II. Natural hybridization among the Pinus rigida–serotina complex, P. taeda and P. echinata. Ann Mo Bot Gard 60:192–203
Soliman MH, Gad Mervat MA, Hussein HM, Mohamed AS (2010) Biochemical and molecular genetic evaluation of some conifers genetic resources. J Am Sci 6(12):1498–1509
Szmidt AE, Wang X–R, Lu M–Z (1996) Empirical assessment of allozyme and RAPD variation in Pinus sylvestris (L.) using haploid tissue analysis. Heredity 76:412–420
Tóth EG, Szilágyi K, Patyi A, György Z (2022) Genetic diversity in a historic lime tree allée of Széchenyi Castle in Nagycenk, Hungary. Genet Resour Crop Evol 69(4):1407–1418
Un–Hyang Ho. Jung Sam Kye. Song Im Choe. Jong Ho Kim. Myong Ho Kim (2021) molecular distinction among mulberry (Morus spp.) species and varieties cultivated in the democratic people’s Republic of Korea.Genet Resour Crop Evol68:3103–3114
Un–Hyang, Ho Jong–Hyang Ri, Chol–Jun Ri (2022)b identification of new stock (Matthiola incana R. Br) cultivars with high fertility through morphological and molecular markers.Genet Resour Crop Evol69(4):2719–2730, https://doi.org/10.1007/s10722-022-01392-9
Un–Hyang, Ho, Sam–Rang Song (2020) Did genetic lineage divergence or spatial environmental variance lead to global subspecies differentiation of northern goshawk (Accipiter gentilis)? Anim Biology 70:289–308
Un–Hyang Ho Sam–Rang, Song Hak–Song, Pak K, Kim Tong–Su Ho, Il–Yop Ju (2022)a genetic evidence of stable northward extension of Pinus thunbergii Parl. Forests in the democratic people’s Republic of Korea.Genet Resour Crop Evol69(4):2105–2114, https://doi.org/10.1007/s10722-022-01359-w
Watanabe A, Shiraishi S, Kawase E, Toda T, Nasu T (1996) Genome analysis of Pinus X densi–thunbergii UYEKI using DNA molecular markers.–Verification of its hybridity. J Jpn For Soc 78:293–300
Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:653l–6535
Yeh FC, Boyle T, Yang R–C, Ye ZMJX (2000) POPGENE, version 1.32. Department of Renewable Resources, University of Alberta, Edmonton, AB, Canada
Zhang ZY, Chen YY, Li DZ (2005) Detection of low genetic variation in a critically endangered chinese pine, Pinus squamata, using RAPD and ISSR markers. Biochem Genet 43:239–249
Zobel BJ (1953) Are there natural loblolly–shortleaf pine hybrids? J For 51:494–495
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We thank all researchers of Forest Research Institute who helped pine sample collection.
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Un–Hyang Ho conceptualized and designed the study, Kang–Song Ju conducted the experiments, and Song–Hyok Pak and Jong–Gum Ri and Myong–Sik Ho analysed the data; Un–Hyang Ho and Kang–Song Ju collected data and wrote the first draft; and all authors contributed substantially to revisions.
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Ho, U., Ju, K., Pak, S. et al. Genetic relationship between Pinus species (P. densiflora, P. thunbergii, P. thunbergii ‘Kumyahuksong’) in the democratic people’s Republic of Korea. Biologia 78, 2657–2665 (2023). https://doi.org/10.1007/s11756-023-01426-2
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DOI: https://doi.org/10.1007/s11756-023-01426-2