Skip to main content
SpringerLink
Log in

Phylogeography of the Korean pine (Pinus koraiensis) in northeast Asia: inferences from organelle gene sequences

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Range-wide genetic variation of Korean pine (Pinus koraiensis) was assessed using maternally inherited mtDNA and paternally inherited cpDNA for 16 natural populations throughout northeast Asia in order to study its phylogeographical history during the Quaternary. The cpDNA variation indicated that there was no difference between populations on the Asian continent and those in the Japanese archipelago. In contrast, the mtDNA variation indicated that there was significant difference between the populations from the two regions, with each region having a different lineage. The continental populations exhibited no diversity in the mtDNA examined despite the species’ current extensive range and large populations. Conversely, while the Korean pine is rare in Japan, the Japanese populations exhibited greater levels of mtDNA diversity (H T = 0.502). The higher mtDNA diversity and evidence from numerous Korean pine macrofossil remains dated to the Pleistocene and recovered various sites in Japan suggest that the Japanese archipelago once served as a refugium to a much larger Korean pine population with a more extensive range than is the case today. The presence of the single mtDNA haplotype across the Asian continent suggests that the present widespread populations could have expanded from a single refugium population after the last glacial periods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aizawa M, Yoshimaru H, Saito H, Katsuki T, Kawahara T, Kitamura K, Shi F, Kaji M (2007) Phylogeography of a northeast Asian spruce, Picea jezoensis, inferred from genetic variation observed in organelle DNA markers. Mol Ecol 16:3393–3405

    Article  PubMed  CAS  Google Scholar 

  • Artyukova EV, Kozyrenko MM, Gorovoy PG, Zhuravlev YN (2009) Plastid DNA variation on highly fragmented populations of Microbiota decussata Kom. (Cupressaceae), an endemic to Sikhote Alin Mountains. Genetica 137:201–212

    Article  PubMed  Google Scholar 

  • Bai WN, Liao WJ, Zhang DY (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

    Article  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  PubMed  CAS  Google Scholar 

  • Burban C, Petit RJ (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Mol Ecol 12:1487–1495

    Article  PubMed  CAS  Google Scholar 

  • Chen K, Abbott RJ, Milne RI, Tian XM, Liu J (2008) Phylogeography of Pinus tabulaeformis Carr. (Pinaceae), a dominant species of coniferous forest in northern China. Mol Ecol 17:4276–4288

    Article  PubMed  CAS  Google Scholar 

  • Chen MM, Feng F, Sui X, Li MH, Zhao D, Han S (2010) Constructing of a framework map for Pinus koraiensis Sieb. et Zucc. using SRAP, SSR and ISSR markers. Trees 24:685–693

    Article  CAS  Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    Article  PubMed  CAS  Google Scholar 

  • Dobson M, Kawamura Y (1998) Origin of the Japanese land mammal fauna: allocation of extant species to historically based categories. Quat Res 37:385–395

    Article  Google Scholar 

  • Du FK, Petit RJ, Liu JQ (2009) More introgression with less gene flow: chloroplast vs. mitochondrial DNA in the Picea asperata complex in China, and comparison with other conifers. Mol Ecol 18:1396–1407

    Article  PubMed  CAS  Google Scholar 

  • Duff RJ, Nickrent DL (1999) Phylogenetic relationships of land plants using mitochondrial small-subunit rDNA sequences. Amer J Bot 86:372–386

    Article  CAS  Google Scholar 

  • Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351

    Article  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Feng F, Han S, Wang H (2006) Genetic diversity and genetic differentiation of natural Pinus koraiensis population. J For Res 17:21–24

    Article  Google Scholar 

  • Feng F, Chen M, Zhang D, Sui X, Han S (2009) Application of SRAP in the genetic diversity of Pinus koraiensis of different provenances. Afr J Biotech 8:1000–1008

    CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hallatschek O, Nelson DR (2008) Gene surfing in expanding populations. Theor Popul Biol 73:158–170

    Article  PubMed  Google Scholar 

  • Hamilton M (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    PubMed  CAS  Google Scholar 

  • Hamrick JL, Godt MLW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New For 6:95–124

    Article  Google Scholar 

  • Harrison SP, Yu C, Takahara H, Prentice IC (2001) Palaeovegetation: diversity of temperate plants in East Asia. Nature 413:129–130

    Article  PubMed  CAS  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hu LJ, Uchiyama K, Shen HL, Saito Y, Tsuda Y, Ide Y (2008) Nuclear DNA microsatellites reveal genetic variation but a lack of phylogeographical structure in an endangered species, Fraxinus mandshurica, across North-east China. Ann Bot 102:195–205

    Article  PubMed  Google Scholar 

  • Hutchins HE, Hutchins SA, Liu B (1996) The role of birds and mammals in Korean pine (Pinus koraiensis) regeneration dynamics. Oecologia 107:120–130

    Article  Google Scholar 

  • Ishikawa Y, Krestov PV, Namikawa K (1999) Disturbance history and tree establishment in old-growth Pinus koraiensis-hardwood forests in the Russian Far East. J Veg Sci 10:439–448

    Article  Google Scholar 

  • Jaramillo-Correa JP, Bousquet J, Beaulieu J, Isabel N, Perron M, Bouillé M (2003) Cross-species amplification of mitochondrial DNA sequence-tagged-site markers in conifers: the nature of polymorphism and variation within and among species in Picea. Theor Appl Genet 106:1353–1367

    PubMed  CAS  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Bousquet J (2004) Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Mol Ecol 13:2735–2747

    Article  PubMed  CAS  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Ledig FT, Bousquet J (2006) Decoupled mitochondrial and chloroplast DNA population structure reveals Holocene collapse and population isolation in a threatened Mexican-endemic conifer. Mol Ecol 15:2787–2800

    Article  PubMed  CAS  Google Scholar 

  • Kim ZS, Lee SW, Lim JH, Hwang JW, Kwon KW (1994) Genetic diversity and structure of natural populations of Pinus koraiensis (Sieb. et Zucc.) in Korea. For Genet 1:41–49

    Google Scholar 

  • Kim ZS, Hwang JW, Lee SW, Yang C, Gorovoy PG (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

    Google Scholar 

  • Kong WS, Watts D (1993) Evergreen arboreal arctic-alpine and alpine plants and their environments. In: Kong WS, Watts D (eds) The plant geography of Korea with an emphasis on the alpine zones. Geobotany, vol 19. Kluwer, Dordrecht, pp 105–140

  • Kremenetski CV, Liu K, MacDonald GM (1998) The late Quaternary dynamics of pines in northeast Asia. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge

    Google Scholar 

  • Krestov PV (2003) Forest vegetation of easternmost Russia (Russian Far East). In: Kolbek J, Šrůtek M, Box EO (eds) Forest vegetation of northeast Asia. Geobotany, vol 28, Kluwer, Dordrecht, pp 93–180

  • Lascoux M, Palmé AE, Cheddadi R, Latta RG (2004) Impact of ice ages on the genetic structure of trees and shrubs. Phil Trans R Soc Lond B 359:197–207

    Article  Google Scholar 

  • Liepelt S, Bialozyt R, Ziegenhagen B (2002) Wind-dispersed pollen mediates postglacial gene flow among refugia. Proc Natl Acad Sci USA 100:10824–10829

    Google Scholar 

  • Meng L, Yang R, Abbott RJ, Miehe G, Hu T, Liu J (2007) Mitochondrial and chloroplast phylogeography of Picea crassifolia Kom. (Pinaceae) in the Qinghai-Tibetan Plateau and adjacent highlands. Mol Ecol 16:4128–4137

    Article  PubMed  CAS  Google Scholar 

  • Miki S (1956) Remains of Pinus koraiensis S. et Z. and associated remains in Japan. Bot Mag Tokyo 69:446–454

    Google Scholar 

  • Miyaki M (1987) Seed dispersal of the Korean pine, Pinus koraiensis, by the red squirrel, Sciurus vulgaris. Ecol Res 2:147–157

    Article  Google Scholar 

  • Momohara A, Mizuno K, Okitsu S (1997) Plant macrofossil assemblages in a latest early Pleistocene cold stage from upper member of the Shobudani formation, southwestern Japan. Jpn J Hist Bot 5:29–37 (in Japanese with English summary)

    Google Scholar 

  • Morita Y (2000) The vegetation history of the subalpine zone in Japan since Last Glacial period–Were the forest zones higher than they are at present during the Climatic Optimum period?–. Jpn J Hist Bot 9:3–20 (in Japanese with English summary)

    Google Scholar 

  • Muir G, Schlötterer C (2005) Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14:549–561

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Ohshima K (1990) The history of straits around the Japanese islands in the late-Quaternary. Quat Res 29:193–208 (in Japanese with English summary)

    Article  Google Scholar 

  • Okitsu S, Momohara A (1997) Distribution of Pinus koraiensis Sieb. et Zucc. in Japan. Tech Bull Fac Hort Chiba Univ 51:137–145 (in Japanese with English summary)

    Google Scholar 

  • Pleines T, Jakob SS, Blattner FR (2009) Application of non-coding DNA regions in intraspecific analyses. Plant Syst Evol 282:281–294

    Article  CAS  Google Scholar 

  • Polezhaeva MA, Lascoux M, Semerikov VL (2010) Cytoplasmic DNA variation and biogeography of Larix Mill. in Northeast Asia. Mol Ecol 19:1239–1252

    Article  PubMed  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered vs. unordered alleles. Genetics 144:1237–1245

    PubMed  CAS  Google Scholar 

  • Potenko VV, Velikov AV (1998) Genetic diversity and differentiation of natural populations of Pinus koraiensis (Sieb. et Zucc.) in Russia. Silvae Genet 47:202–208

    Google Scholar 

  • Qiu YX, Fu CX, Comes HP (2011) 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

    Article  PubMed  Google Scholar 

  • Ren G, Zhang L (1998) A preliminary mapped summary of Holocene pollen data for Northeast China. Quat Sci Rev 17:669–688

    Article  Google Scholar 

  • Stebich M, Mingram J, Han J, Liu J (2009) Late Pleistocene spread of (cool-)temperate forests in Northeast China and climate changes synchronous with the North Atlantic region. Global Planet Change 65:56–70

    Article  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tsutsui K, Suwa A, Sawada K, Kato T, Ohsawa TA, Watano Y (2009) Incongruence among mitochondrial, chloroplast and nuclear gene trees in Pinus subgenus Strobus (Pinaceae). J Plant Res 122:509–521

    Article  PubMed  CAS  Google Scholar 

  • Wagner DB (1992) Nuclear, chloroplast and mitochondrial DNA polymorphisms as biochemical markers in population genetic analysis of forest trees. New For 6:373–390

    Article  Google Scholar 

  • Wang XQ, Tank DC, Sang T (2000) Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17:773–781

    Article  PubMed  CAS  Google Scholar 

  • Yano M, Ishikari Teichitai Research Group (1967) Outline of the plants remains from the Quaternary deposits in the Ishikari Plain Hokkaido. Quat Res 7:41–48 (in Japanese with English summary)

    Google Scholar 

  • Zhou YF, Abbott RJ, Jiang ZY, Du FK, Milne RI, Liu JQ (2010) Gene flow and species delimitation: a case study of two pine species with overlapping distributions in southeast China. Evolution 64:2342–2352

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Y. Tsuda (Uppsala University), Y. Tsumura, S. Kikuchi, Y. Taguchi and Y. Moriguchi (Department of Forest Genetics, Forestry and Forest Products Research Institute, FFPRI) for their technical advice on experimental design and data analyses. We are grateful to Y.-P. Hong and K.N. Hong (Korea Forest Research Institute) and H. Sugita (FFPRI) for fruitful discussion. We also thank the regional offices of the Forestry Agency, Japan, and prefectural offices for permitting sampling. This study was financially supported by a Grant-in-Aid for Scientific Research (#19780111 and #21780141) from the Ministry of Education, Culture, Sports, Science and Technology.

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Department of Forest Science, Faculty of Agriculture, Utsunomiya University, 350, Mine-machi, Utsunomiya, Tochigi, 321-8505, Japan

    Mineaki Aizawa

  2. Division of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul, 136-713, Korea

    Zin-Suh Kim

  3. Forestry and Forest Products Research Institute, Tama Forest Science Garden, 1833-81, Todori-machi, Hachioji, Tokyo, 193-0843, Japan

    Hiroshi Yoshimaru

Authors
  1. Mineaki Aizawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zin-Suh Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroshi Yoshimaru
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mineaki Aizawa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aizawa, M., Kim, ZS. & Yoshimaru, H. Phylogeography of the Korean pine (Pinus koraiensis) in northeast Asia: inferences from organelle gene sequences. J Plant Res 125, 713–723 (2012). https://doi.org/10.1007/s10265-012-0488-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-012-0488-4

Keywords

Search

Navigation