Skip to main content
SpringerLink
Log in

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

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

Abstract

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.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Barrett SCH (1998) The reproductive biology and genetics of island plants. In: Grand PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 18–34

    Google Scholar 

  • 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 102–123

    Google Scholar 

  • Beaumont MA (2010) Approximate Bayesian computation in evolution and ecology. Annu Rev of Ecol Evol Syst 41:379–405

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Csilléry K, François O, Blum MGB (2012) abc: an R package for approximate Bayesian computation (ABC). Meth Ecol Evol 3:475–479

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dussert Y, Snirc A, Robert T (2015) Inference of domestication history and differentiation between early- and late-flowering varieties in pearl millet. Mol Ecol 24:1387–1402

    Article  CAS  PubMed  Google Scholar 

  • 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 92:832–839

    Article  PubMed  Google Scholar 

  • Estoup A, Jarne P, Cornuet J-M (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Foll M (2011) fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex scenarios. Bioinfomatics 27:1332–1334

    Article  CAS  Google Scholar 

  • 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 10:564–567

    Article  PubMed  Google Scholar 

  • Excoffier L, Estoup A, Cornuet J-M (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:399–410

    Article  CAS  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm, March 25, 2017

  • 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 1:345–349

    Article  CAS  Google Scholar 

  • 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 122:269–282

    Article  CAS  PubMed  Google Scholar 

  • 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 79:141‒149

    Article  Google Scholar 

  • 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)

    Article  Google Scholar 

  • Iwatsuki K (1999) Anacardiaceae. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, vol. IIc. Kodansha, Tokyo, pp 58–59

    Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • 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 222–227

    Google Scholar 

  • Masaki Y (1938) Toxicodendron succedaneum and sumac wax in Japan [*in Japanese, title is a tentative translation by the author]. Meibundo, Tokyo

    Google Scholar 

  • Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404

    Article  Google Scholar 

  • Muse SV (2000) Examining rates and patterns of nucleotide substitution in plants. Plant Mol Biol 42:25–43

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 47:416–430

    Article  Google Scholar 

  • 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 1:1–24

    Google Scholar 

  • Petit RJ, Bodenes C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164

    Article  CAS  Google Scholar 

  • Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11

  • Potts BM, Reid JB (1988) Hybridization as a dispersal mechanism. Evolution Int J org Evolution 42:1245–1255

    Article  Google Scholar 

  • Prichard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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 365–386

    Google Scholar 

  • 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 21:3823–3838

    Article  PubMed  Google Scholar 

  • 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 

  • 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 63:823–831

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J org Evol 38:1358–1370

    CAS  Google Scholar 

  • 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—1360

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Forest Tree Breeding Center, Forestry and Forest Products Research Institute (FFPRI), 3809-1 Ishi, Juo, Hitachi, Ibaraki, 319-1301, Japan

    Yuichiro Hiraoka

  2. Gifu Academy of Forest Science and Culture, 88 Sodai, Mino, Gifu, 501-3714, Japan

    Ichiro Tamaki

  3. Faculty of Agriculture, Kyushu University, Hakozaki 6-10-1, Higashi-ku, Fukuoka, 812-8581, Japan

    Atsushi Watanabe

Authors
  1. Yuichiro Hiraoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ichiro Tamaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atsushi Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuichiro Hiraoka.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Funding

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 12242 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hiraoka, Y., Tamaki, I. & Watanabe, A. The origin of wild populations of Toxicodendron succedaneum on mainland Japan revealed by genetic variation in chloroplast and nuclear DNA. J Plant Res 131, 225–238 (2018). https://doi.org/10.1007/s10265-017-0992-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-017-0992-7

Keywords

Search

Navigation