Skip to main content
SpringerLink
Log in

Geographic patterns of genetic variation in nuclear and chloroplast genomes of two related oaks (Quercus aliena and Q. serrata) in Japan: implications for seed and seedling transfer

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

In this study, we assessed geographic patterns of genetic variations in nuclear and chloroplast genomes of two related native oaks in Japan, Quercus aliena and Q. serrata, in order to facilitate development of genetic guidelines for transfer of planting stocks for each species. A total of 12 populations of Q. aliena and 44 populations of Q. serrata were analyzed in this study. Genotyping of nuclear microsatellites in Q. aliena was done with only nine populations (n = 212) due to limited numbers of individuals in two populations, while all 12 populations (n = 89) were used in sequencing chloroplast DNA (cpDNA). In Q. serrata, 43 populations (n = 1032) were genotyped by nuclear microsatellite markers, while cpDNA of 44 populations (n = 350) was sequenced. As anticipated, geographic patterns detected in the variations of Q. aliena’s nuclear genome and its chloroplast haplotype distribution clearly distinguished northern and southern groups of populations. However, those of Q. serrata were inconsistent. The geographic distribution of its chloroplast haplotypes tends to show the predicted differentiation between northern and southern lineages, but geographic signals in the genetic structure of its nuclear microsatellites are weak. Therefore, treating northern and southern regions of Japan as genetically distinct transferrable zones for planting stocks is highly warranted for Q. aliena. For Q. serrata, the strong NE-SW geographic structure of cpDNA should be considered.

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

  • Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Soulé M (ed) Conservation Biology. The science of scarcity and diversity. Sinauer Assoc., Sunderland, pp 57–76

    Google Scholar 

  • Arbogast BS, Kenagy GJ (2001) Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr 28:819–825

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Belahbib N, Pemonge M-H, Ouassou A, Sbay H, Kremer A, Petit RJ (2001) Frequent cytoplasmic exchanges between oak species that are not closely related: and in Morocco. Mol Ecol 10(8):2003–2012

    Article  CAS  PubMed  Google Scholar 

  • Bognoli F, Tsuda Y, Fineschi S, Bruschi P, Magri D, Zhelev P, Paule L, Simeone MC, Gonzalez-Martinez SC, Vendramin GG (2016) Combining molecular and fossil data to infer demographic history of Quercus cerris: insights on European eastern glacial refugia. J Biogeogr 43:679–690

  • Campbell RK (1979) Genecology of Douglas-fir in watershed in the Oregon cascades. Ecology 60:1036–1050

    Article  Google Scholar 

  • Cavender-Bares J, Gonzalez_Rodriguez A, Pahlich A, Koehler K, Nicholas D (2011) Phylogeography and climate niche evolution in live oaks (Quercus series Virentes) from the tropics to the temperate zone. J Biogeogr 38:962–981

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuet JM, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11:401

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornille A, Gladieux P, Smulders MJM, Roldán-Ruiz I, Laurens F, Le Cam B, Nersesyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang X-G, Tenaillon MI, Giraud T, Mauricio R (2012) New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet 8(5):e1002703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Souza RF, Ziroldo BD, Rosetto EF, Cavalheiro AL, Torezan JMD, Vanzela ALL (2012) The use of genetic structure as a guide for seed gathering for forest restoration. Braz J Biosci 10:309–313

    Google Scholar 

  • Dumolin-Lapegue S, Demesure B, Le Corre V, Fineschi S, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146:1475–1487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res. https://doi.org/10.1007/s12686-011-9548-7

  • El Moussadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [(Arganiaspinosa (L.) Skeels)] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Ersts PJ (2006) [Internet] Geographic Distance Matrix Generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation, New York Available from http://biodiversityinformatics.amnh.org/open_source/gdmg.Accessed on 2012-11-22

    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, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferris C, Oliver RP, Davy AJ, Hewitt GM (1993) Native oak chloroplasts reveal an ancient divide across Europe. Mol Ecol 2:337–343

    Article  CAS  PubMed  Google Scholar 

  • Ferris C, King RA, Väinölä R, Hewitt GM (1998) Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland. Heredity 80(5):584–593

    Article  PubMed  Google Scholar 

  • FFPRI (2011) Seedling transfer guideline of Japanese broadleaf tree species based on genetic data. ISBN:978-4-902606-75-1, https://www.ffpri.affrc.go.jp/pubs/chukiseika/documents/2nd-chukiseika20.pdf

  • Gomory D, Hynek V, Paule L (1998) Delineation of seed zones for European beech (Fagus sylvatica L.) in the Czech Republic based on isozyme gene markers. Ann Sci For 55:425–436

    Article  Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available from: http://www2.unil.ch/popgen/softwares/fstat.htmGoudet et al. (2006)

  • Goudet J, Raymond M, de Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guicking D, Fiala B, Blattner F, Slik F, Mohamed M, Weising K (2011) Comparative chloroplast phylogeography of two tropical pioneer trees, Macaranga gigantean and Macaranga pearsonii (Euphorbiaceae). Tree Genet Genomes 7:573–585

    Article  Google Scholar 

  • Hagiwara S (1977) Clines on leaf size of beech Fagus crenata. Species Biol Res 1:39–51 (in Japanese)

    Google Scholar 

  • Hamann A, Gylander T, Chen P (2011) Developing seed zones and transfer guidelines with multivariate regression trees. Tree Genet Genomes 7:399–408

    Article  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Hillis DM, Moritz C (1990) Molecular taxonomy. Sinauer associates, Inc. Publishers, Massachusetts

    Google Scholar 

  • Hiraoka K, Tomaru N (2009a) 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

  • Hiraoka K, Tomaru N (2009b) Genetic structure of Fagus japonica revealed by nuclear microsatellite markers. Int J Plant Sci 170:748–758

    Article  Google Scholar 

  • Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Iwabuchi Y, Hoshino Y, Hukusima T (2006) Intraspecific variation of acorn traits of Quercus serrata Thunb. In Kanto region, central Japan. Veg Sci 23:81–88

    Google Scholar 

  • Iwasaki T, Aoki K, Seo A, Murakami N (2012) Comparative phylogeography of four component species of deciduous broad-leaved forests in Japan based on chloroplast DNA variation. J Plant Res 125:207–221

    Article  PubMed  Google Scholar 

  • Jørgensen MH, Elameen A, Hofman N, Klemsdal S, Malaval S, Fjellheim S (2016) What’s the meaning of local? Using molecular markers to define seed transfer zones for ecological restoration in Norway. Evol Appl 9:673–684. https://doi.org/10.1111/eva.12378

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanno M, Suzuki M (2005) Intraspecific variation of acorn morphology within Quercus aliena Blume in Japan and South Korea. Proceedings of conference OAK 2003 ‘Integration of Silviculture and Genetics in Creating and Sustaining of Oak Forests’ held on 29 Sept. - 3 Oct. 2003 in Tsukuba and Nikko, Japan 153–158

  • Kanno M, Yokoyama J, Suyama Y, Ohyama M, Itoh T, Suzuki M (2004) Geographical distribution of two haplotypes of chloroplast DNA in four oak species (Quercus) in Japan. J Plant Res 117:311–317

    Article  PubMed  Google Scholar 

  • Keir KR, Bemmels JB, Aitken SN (2011) Low genetic diversity, moderate local adaptation, and phylogeographic insights in Cornus nuttallii (Cornaceae). Am J Bot 98:1327–1336

    Article  PubMed  Google Scholar 

  • Kitamura S, Horikawa (1951) On Quercus subgen. Lepidobalanus of Japan, Korea, and North China. Mem Coll Sci Univ Tokyo Ser B 20:20–25

    Google Scholar 

  • Krauss SL, He TH (2006) Rapid genetic identification of local provenance seed collection zones for ecological restoration and biodiversity conservation. J Nat Conserv 14:190–199

    Article  Google Scholar 

  • Krauss SL, Koch JM (2004) Rapid genetic delineation of provenance for plant community restoration. J Appl Ecol 41:1162–1173

    Article  Google Scholar 

  • Kremer A, Petit RJ (1993) Gene diversity in natural populations of oak species. Ann Sci For 50(Suppl 1):186s–202s

    Article  Google Scholar 

  • Langella O (1999) Population 1.2.30 http://bioinformatics.org/~tryphon/populati-ns/

  • Lee SH, You YH (2012) Measurement of ecological niche of Quercus aliena and Q. serrata under environmental factors treatments and its meaning to ecological distribution. J Ecol Field Biol 35:227–234

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–248

    Article  CAS  PubMed  Google Scholar 

  • Maliouchenko O, Palmé AE, Buonamici A, Vendramin GG, Lascoux M (2007) Comparative phylogeography and population structure of European Betula species, with particular focus on B. pendula and B. pubescens. J Biogeogr 34:1601–1610

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Maruyama T, Fuerst TA (1985) Population bottlenecks and non-equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto A, Kawahara T, Kanazashi A, Yoshimaru H, Takahashi M, Tsumura Y (2009) Differentiation of three closely related Japanese oak species and detection of interspecific hybrids using AFLP markers. Botany 87:145–153

    Article  CAS  Google Scholar 

  • McKay JK, Christian E, Harisson S, Rice KJ (2005) “How local is local?” A review of practical and conceptual issues in the genetics of restoration. Restor Ecol 13:432–440

    Article  Google Scholar 

  • Moncada KM, Ehlke NJ, Muehlbauer GJ, Sheaffer CC, Wysw DL, DeHaan LR (2007) Genetic variation in three native plant species across the state of Minnesota. Crop Sci 47:2379–2389

    Article  CAS  Google Scholar 

  • Moritz C (1995) Uses of molecular phylogenies for conservation. Phil Trans R Soc Lond B349:113–118

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  PubMed  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170

    Article  CAS  PubMed  Google Scholar 

  • Nozaki R, Kurohara A, Kamei H (2001) A preliminary study on the Quercus aliena forest: a type of natural forest vegetation on the alluvial plain in Japan. Papers in commemoration of Prof. Dr. Shigetoshi Okuda’s retirement: studies on vegetation of alluvial plains. 23–32 (in Japanese with English abstract)

  • Ohba H (2006) Fagaceae. In: Iwatsuki K, Boufford D, Ohba H (eds) Flora of Japan, volume IIa. Kodansha Ltd., Japan, pp 42–60

    Google Scholar 

  • Ohsawa T, Ide Y (2011) Phylogeographic patterns of highland and lowland plant species in Japan. Alp Bot 121:49–61

    Article  Google Scholar 

  • Ohsawa T, Tsuda Y, Sawada H, Ide Y (2006) Genetic diversity and gene flow of Quercus crispula in a semi-fragmented forest together with neighboring forests. Silvae Genet 55:160–169\

    Google Scholar 

  • Ohsawa T, Tsuda Y, Saito Y, Ide Y (2011) The genetic structure of Quercus crispula in northern Japan as revealed by nuclear simple sequence repeat loci. J Plant Res 124:645–654

    Article  PubMed  Google Scholar 

  • Okaura T, Quang ND, Ubukata M, Harada K (2007) Phylogeographic structure and late Quaternary population history of the Japanese oak Quercus mongolica var. crispula and related species revealed by chloroplast DNA variation. Genes Genet Syst 82:465–477

    Article  CAS  PubMed  Google Scholar 

  • Okumura T, Oki M (1992) Survey on flowering and fruiting of useful broadleaf tree species in deciduous broadleaf tree forest zone. Bulletin of Nagano Prefecture. For Res 6:1–15

    Google Scholar 

  • Ortego J, Noguerales V, Gugger PF, Sork VL (2015) Evolutionary and demographic history of the Californian scrub white oak species complex: an integrative approach. Mol Ecol 24(24):6188–6208

    Article  PubMed  Google Scholar 

  • Petit RJ, Hampe A (2006) Some evolutional consequences of being a tree. Ann Rev Ecol Evol Syst 37:187–214

    Article  Google Scholar 

  • Petit RJ, Kremer A, Wagner DB (1993) Geographic structure of chloroplast DNA polymorphisms in European oaks. Theor Appl Genet 87:122–128

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 4:844–855

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity. I: haploid locus. Theor Appl Genet 90:462–470

    Article  CAS  PubMed  Google Scholar 

  • Prim RC (1957) Shortest connection networks and some generalizations. Bell Syst Tech J 36:1389–1401

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • Rossetto M, Crayn D, Ford A, Ridgeway P, Rymer P (2007) The comparative study of range-wide genetic structure across related co-distributed rainforest trees reveals contrasting evolutionary histories. Aust J Bot 55:416–424

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing the phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    Article  CAS  PubMed  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Tani A, Kawawata (2008) Isoprene emission from the major native Quercus spp. in Japan. Atmos Environ 42:4540–4550

    Article  CAS  Google Scholar 

  • Taoda H (2005) Integration of silviculture and genetics in creating and sustaining of oak forests. Proceedings of OAK 2003 FFPRI Scientific Meeting Report 3 ISSN 1341–1969. Takeuchi, A., MD Co., Ltd., Tsukuba 26 September 2005

  • Templeton AR (1986) Coadaptation and outbreeding depression. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 105–116

    Google Scholar 

  • Tomaru N, Mitsutsuji T, Takahashi M, Tsumura Y, Uchida K, Ohba K (1997) Genetic diversity in Japanese beech, Fagus crenata: influence of the distributional shift during the late-Quaternary. Heredity 78:241–251

    Article  Google Scholar 

  • Tomaru N, Takahashi M, Tsumura Y, Takahashi M, Ohba K (1998) Intraspecific variation and phylogeographic patterns of Fagus crenata (Fagaceae) mitochondrial DNA. Am J Bot 85:629–636

    Article  CAS  PubMed  Google Scholar 

  • Toyama H, Yahara T (2009) Comparative phylogeography of two closely related Viola species occurring in contrasting habitats in Japanese archipelago. J Plant Res 122:389–401

    Article  CAS  PubMed  Google Scholar 

  • Tsuda Y, Nakao K, Ide Y, Tsumura Y (2015) The population demography of Betula maximowicziana, a cool-temperate tree species in Japan, in relation to the last glacial period: its admixture-like genetic structure is the result of simple population splitting not admixing. Mol Ecol 24:1403–1418

    Article  CAS  PubMed  Google Scholar 

  • Tsukada M (1982a) Late quaternary shift of Fagus distribution. Bot Mag Tokyo 95:203–217

    Article  Google Scholar 

  • Tsukada M (1982b) Late quaternary development of Fagus forest in the Japanese archipelago. Jpn J Ecol 32:113–118

    Google Scholar 

  • Tsumura Y, Suyama Y (eds) (2015) Seedling transfer guideline of Japanese tree species. Bun-ichi Co Ltd, Tokyo, p 176 ISBN-10: 482996524X, (in Japanese)

    Google Scholar 

  • Tsumura Y, Uchiyama K, Moriguchi Y, Kimura MK, Ueno S, Ihara-Ujino T (2014) Genetic differentiation and evolutionary adaptation in Cryptomeria japonica. Genes Genomes Genet 4:2389–2402

    Google Scholar 

  • Ueno S, Tsumura Y (2008) Development of microsatellite markers for Quercus mongolica var. crispula by database mining. Conserv Genet 9:1083–1085

    Article  CAS  Google Scholar 

  • Ueno S, Taguchi Y, Tsumura Y (2008) Microsatellite markers derived from Quercus mongolica var. crispula (Fagaceae) inner bark expressed sequence tags. Genes Genet Syst 83:179–187

    Article  CAS  PubMed  Google Scholar 

  • Ueno S, Aoki K, Tsumura Y (2009a) Generation of expressed sequence tags and development of microsatellite markers for Castanopsis sieboldii var. sieboldii (Fagaceae). Ann For Sci 66:509. https://doi.org/10.1051/forest/2009037

    Article  Google Scholar 

  • Ueno S, Taguchi Y, Tomaru N, Tsumura Y (2009b) Development of EST-SSR markers from inner bark of cDNA library of Fagus crenata (Fagaceae). Conserv Genet 10:1477–1485

    Article  CAS  Google Scholar 

  • Van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25(2/3):233

    Article  Google Scholar 

  • Vander Mijnsbrugge K, Bischoff A, Smith B (2010) A question of origin: where and how to collect seed for ecological restoration. Basic Appl Ecol 11:300–311

    Article  Google Scholar 

  • Weels G, Zawko G, Rosetto M, Dixon K (2003) A molecular approach to provenance delineation for the restoration of hummock grasslands (Triodia spp.) in arid-tropical Australia. Ecol Manage Restor 4:S60–S68

    Article  Google Scholar 

  • Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci 88(6):2540–2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354

    Article  CAS  Google Scholar 

  • Yang J, Di X, Meng X, Fen L, Lui Z, Zhao G (2016) Phylogeography and evolution of two closely related oal species (Quercus) from north and northeast China. Tree Genet Genome 12:89

  • Yasue M, Ogiyama K, Suto S, Tsukahara H, Miyahara F, Ohba K (1987) Geographical differentiation of natural Cryptomeria stands analyzed by diterpene hydrocarbon constituents of individual trees. J Jpn For Soc 69:152–156

    Google Scholar 

  • You YH, Gi KJ, Han D, Kwak YS, Kim JH (1995) Succession and heterogeneity of plant community in Mt. Yongam, Kwangnung experimental forest. Kor J Ecol 18:89–97

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank H. Nishikawa, K. Kitamura, H. Koyama, S. Kanetani, M. Saito, M. Aizawa, K. Ishida, Y. Tsuda, T. Kawahara, A. Tamura, T. Nagamitsu, and S. Fukushima for sampling of materials, and Y. Taguchi for assistance with laboratory work.

Funding

This research was supported by a grant for research on Genetic Guidelines for Restoration Programs using Genetic Diversity Information (2005–2009) from the Ministry of Environment, Japan.

Author information

Authors and Affiliations

  1. College of Forestry and Natural Resources, University of the Philippines Los Baños, 4031, Laguna, Philippines

    Lerma San Jose-Maldia

  2. Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan

    Lerma San Jose-Maldia, Asako Matsumoto, Saneyoshi Ueno, Ayako Kanazashi, Hiroshi Yoshimaru & Yoshihiko Tsumura

  3. IDEA Consultants, Inc. Tohoku Branch, Natural Environment Conservation, Sendai, Japan

    Munetake Kanno

  4. Hokkaido University of Education Sapporo, 5-3-1 Ainosato, Kita-ku, Sapporo, 002-8502, Japan

    Kanji Namikawa

  5. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Yoshihiko Tsumura

Authors
  1. Lerma San Jose-Maldia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Asako Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saneyoshi Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ayako Kanazashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Munetake Kanno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kanji Namikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroshi Yoshimaru
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yoshihiko Tsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoshihiko Tsumura.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

The sequences were deposited in the DNA Data Bank of Japan. A full list of accession numbers for haplotypes of individuals is included in the supplementary information (Online Resource 3).

Additional information

Communicated by A. Kremer

Electronic supplementary material

Online Resource 1

(DOCX 25 kb)

Online Resource 2

(DOCX 21 kb)

Online Resource 3a

(DOCX 21 kb)

Online Resource 3b

(DOCX 20 kb)

Online Resource 4

(DOCX 25 kb)

Online Resource 5

(DOCX 16 kb)

Online Resource 6a

(DOCX 482 kb)

Online Resource 6b

(DOCX 18 kb)

Online Resource 7a

(DOCX 93 kb)

Online Resource 7b

(DOCX 17 kb)

Online Resource 8a

(DOCX 651 kb)

Online Resource 8b

(DOCX 20 kb)

Online Resource 9

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

San Jose-Maldia, L., Matsumoto, A., Ueno, S. et al. Geographic patterns of genetic variation in nuclear and chloroplast genomes of two related oaks (Quercus aliena and Q. serrata) in Japan: implications for seed and seedling transfer. Tree Genetics & Genomes 13, 121 (2017). https://doi.org/10.1007/s11295-017-1202-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-017-1202-4

Keywords

Search

Navigation