Journal of Plant Research

, Volume 131, Issue 2, pp 225–238 | Cite as

The origin of wild populations of Toxicodendron succedaneum on mainland Japan revealed by genetic variation in chloroplast and nuclear DNA

  • Yuichiro Hiraoka
  • Ichiro Tamaki
  • Atsushi Watanabe
Regular Paper


Toxicodendron succedaneum: (L.) Kuntze is a tree cultivated for the production of sumac wax, which is extracted from the mesocarp. There are several hypotheses regarding the origin of T. succedaneum on mainland Japan. In this study, the geographical distribution of genetic variation in 13 wild populations on Honshu, Shikoku, Kyushu, and Ryukyu Islands, Japan was investigated and compared with that of individuals from continental Asia. Seven chloroplast DNA haplotypes of T. succedaneum were observed in Japan and could be divided into three lineages based on relatedness between haplotypes. One of these lineages was also observed in continental Asia, and the others were genetically distant from the haplotypes that originated on the continent, with one considered to have originated on the Ryukyu Islands, and the other on mainland Japan. The genetic diversity of both chloroplast and nuclear DNA was lower in populations from Ryukyu Islands than in populations from mainland Japan. Bayesian clustering based on nuclear genotypes showed a clear difference between the groups from Ryukyu Islands and mainland Japan. Based on approximate Bayesian computation analysis of polymorphic data for both genomes, it was inferred that wild populations of T. succedaneum on mainland Japan consist of both lineages with natural distribution on mainland Japan and those introduced from Ryukyu Islands and continental Asia.


Approximate Bayesian computation Artificial movement Chloroplast haplotype Cultivated tree Nuclear SSR marker 



We are grateful to Drs. M. Suzuki and T. Tanaka for sampling the materials used in this study. We also thank Mr. M. Ogata, Mr. K. Miyahira, the members of the Kyushu Regional Breeding Office (Forest Tree Breeding Center), Fukuoka Prefecture and Chiba Prefecture, for their assistance in the field. We also thank Dr. K. Mishima and the members of the Forest Tree Breeding Center for their support with experiments. We also thank Drs. S. Shiraishi, M. Tamura, and M. Takahashi for helpful advice.

Conflict of interest

The authors declare that they have no conflicts of interest.


This research was supported by funds from the ordinary budget of the Forestry and Forest Products Research Institute (FFPRI).

Supplementary material

10265_2017_992_MOESM1_ESM.pdf (12 mb)
Supplementary material 1 (PDF 12242 KB)


  1. Barrett SCH (1998) The reproductive biology and genetics of island plants. In: Grand PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 18–34Google Scholar
  2. Barton NH (1998) Natural selection and random genetic drift as causes of evolution on islands. In: Grand PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 102–123Google Scholar
  3. Beaumont MA (2010) Approximate Bayesian computation in evolution and ecology. Annu Rev of Ecol Evol Syst 41:379–405CrossRefGoogle Scholar
  4. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  5. Csilléry K, François O, Blum MGB (2012) abc: an R package for approximate Bayesian computation (ABC). Meth Ecol Evol 3:475–479Google Scholar
  6. Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008CrossRefPubMedPubMedCentralGoogle Scholar
  7. Dussert Y, Snirc A, Robert T (2015) Inference of domestication history and differentiation between early- and late-flowering varieties in pearl millet. Mol Ecol 24:1387–1402CrossRefPubMedGoogle Scholar
  8. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839CrossRefPubMedGoogle Scholar
  9. Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604CrossRefPubMedGoogle Scholar
  10. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  11. Excoffier L, Foll M (2011) fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex scenarios. Bioinfomatics 27:1332–1334CrossRefGoogle Scholar
  12. Excoffier L, Lischer HE (2010) Arlquin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  13. Excoffier L, Estoup A, Cornuet J-M (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738CrossRefPubMedPubMedCentralGoogle Scholar
  14. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  15. Fiorentino F, Magli MC, Podini D, Ferraretti AP, Nuccitelli A, Vitale N, Baldi M, Gianaroli L (2003) The minisequencing method: an alternative strategy for preimplantation genetic diagnosis of single gene disorders. Mol Hum Reprod 9:399–410CrossRefPubMedGoogle Scholar
  16. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  17. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from, March 25, 2017Google Scholar
  18. Grivet D, Heinze B, Vendramin GG, Petit RJ (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1:345–349CrossRefGoogle Scholar
  19. Hiraoka K, Tomaru N (2009) Genetic divergence in nuclear genomes between populations of Fagus crenata along the Japan Sea and Pacific sides of Japan. J Plant Res 122:269–282CrossRefPubMedGoogle Scholar
  20. Hiraoka Y, Watanabe A (2010) Development and characterization of microsatellites, clone identification, and determination of genetic relationships among Rhus succedanea L. individuals. J Jpn Soc Hortic Sci 79:141‒149CrossRefGoogle Scholar
  21. Hiraoka Y, Watanabe A (2011) Comparisons of chloroplast haplotypes in Toxicodendron succedaneum (L.) Kuntze among local cultivars and candidates for superior trees in Japan and wild individuals from the Asian Continent and Okinawa Island. J Jpn For Soc 93:200‒204 (in Japanese with English summary)CrossRefGoogle Scholar
  22. Iwatsuki K (1999) Anacardiaceae. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, vol. IIc. Kodansha, Tokyo, pp 58–59Google Scholar
  23. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543CrossRefGoogle Scholar
  24. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  25. Katsuta M (1998) Rhus Linn. (Sumac). In: Katsuta M, Mori T, Yokoyama T. Seed of forest tree in Japan [*in Japanese, the book title is a tentative translation by the author], Society of Forest Tree Breeding, Tokyo, pp 222–227Google Scholar
  26. Masaki Y (1938) Toxicodendron succedaneum and sumac wax in Japan [*in Japanese, title is a tentative translation by the author]. Meibundo, TokyoGoogle Scholar
  27. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404CrossRefGoogle Scholar
  28. Muse SV (2000) Examining rates and patterns of nucleotide substitution in plants. Plant Mol Biol 42:25–43CrossRefPubMedGoogle Scholar
  29. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  30. Nie Z, Sun H, Meng Y, Wen J (2009) Phylogenetic analysis of Toxicodendron (Anacardiaceae) and its biogeographic implications on the evolution of north temperate and tropical intercontinental disjunctions. J Syst Evol 47:416–430CrossRefGoogle Scholar
  31. Noguchi K (1977) Development of Toxicodendron succedaneum cultivation and dispersion of elite cultivars in Japan [*in Japanese, title is a tentative translation by the author]. Rekishigaku Chirigaku Nenpo 1:1–24Google Scholar
  32. Petit RJ, Bodenes C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164CrossRefGoogle Scholar
  33. Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11Google Scholar
  34. Potts BM, Reid JB (1988) Hybridization as a dispersal mechanism. Evolution Int J org Evolution 42:1245–1255CrossRefGoogle Scholar
  35. Prichard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  36. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  37. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, pp 365–386Google Scholar
  38. Sakaguchi S, Qiu Y-X, Liu Y-H, Qi X-S, Kim S-H, Han J, Takeuchi Y, Worth JRP, Yamasaki M, Sakurai S, Isagi Y (2012) 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 21:3823–3838CrossRefPubMedGoogle Scholar
  39. Shiraishi S, Watanabe A (1995) Identification of chloroplast genome between Pinus densiflora Sieb. et Zucc. and P. thunbergii Parl. based on the polymorphism in rbcL gene. J Jpn For Soc 77:429–436 (Japanese with English summary)Google Scholar
  40. Tamaki I, Kuze T, Hirota K, Mizuno M (2016) Genetic variation and population demography of the landrace population of Camellia sinensis in Kasuga, Gifu Prefecture, Japan. Gen Res Crop Evol 63:823–831Google Scholar
  41. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J org Evol 38:1358–1370Google Scholar
  42. Zhai S-N, Comes HP, Nakamura K, Yan H-F, Qiu Y-X (2012) Late Pleistocene lineage divergence among populations of Neolitsea sericea (Lauraceae) across a deep sea-barrier in the Ryukyu Islands. J Biogeogr 39:1347—1360Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Yuichiro Hiraoka
    • 1
  • Ichiro Tamaki
    • 2
  • Atsushi Watanabe
    • 3
  1. 1.Forest Tree Breeding CenterForestry and Forest Products Research Institute (FFPRI)HitachiJapan
  2. 2.Gifu Academy of Forest Science and CultureMinoJapan
  3. 3.Faculty of AgricultureKyushu UniversityHigashi-kuJapan

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