Tree Genetics & Genomes

, 13:91 | Cite as

Genetic diversity and population structure in the narrow endemic Chinese walnut Juglans hopeiensis Hu: implications for conservation

Original Article
Part of the following topical collections:
  1. Population structure

Abstract

The conservation of narrow endemic species relies on accurate information regarding their population structure. Juglans hopeiensis Hu (Ma walnut), found only in Hebei province, Beijing, and Tianjin, China, is a threatened tree species valued commercially for its nut and wood. Sequences of two maternally inherited mitochondrial markers and two maternally inherited chloroplast intergenic spacers, three nuclear DNA sequences, and allele sizes from 11 microsatellites were obtained from 108 individuals of J. hopeiensis, Juglans regia, and Juglans mandshurica. Haplotype networks were constructed using NETWORK. Genetic diversity, population differentiation, and analysis of molecular variance (AMOVA) were used to determine genetic structure. MEGA was used to construct phylogenetic trees. Genetic diversity of J. hopeiensis was moderate based on nuclear DNA, but low based on uniparentally inherited mitochondrial DNA and chloroplast DNA. Haplotype networks showed that J. hopeiensis haplotypes were different than haplotypes found in J. regia and J. mandshurica. Allelic variants in nuclear genes that were shared among J. hopeiensis populations were not found in J. regia or J. mandshurica. Sampled populations of J. hopeiensis showed clear genetic structure. The maximum parsimony (MP) tree showed J. hopeiensis to be distinct from J. mandshurica but threatened by hybridization with J. regia and J. mandshurica. J. hopeiensis populations are strongly differentiated from sympatric Juglans species, but they are threatened by small population sizes and hybridization.

Keywords

Chinese walnut Hybridization Conservation Genetic differentiation Microsatellites Juglans regia Juglans mandshurica 

Supplementary material

11295_2017_1172_MOESM1_ESM.pdf (1.1 mb)
Fig. S1Nucleotide sequence variation of (a) mtDNA(3-9 and nad5). (b) cpDNA (trnS-G and trnL-F). (c) 15R-8. (d) ITS. (e) Jr5680. Hap=haplotype. The yellow color indicates that “G”, green color indicates that “T”, red color indicates that “A”, blue color indicates that “C” which is different with the consensus sequence, respectively. (PDF 1109 kb)
11295_2017_1172_MOESM2_ESM.pdf (404 kb)
Fig. S2Maximum parsimony (MP) trees for all 17 populations of J. regia, J. hopeiensis, and J. mandshurica based on (a) mtDNA (3-9 and nad5), (b) cpDNA (trnS-G and trnL-F), and (c) nrDNA (ITS, 15R-8, and Jr5680) sequences. (PDF 404 kb)
11295_2017_1172_MOESM3_ESM.pdf (450 kb)
Fig. S3Mismatch distribution analysis for mtDNA(nad5 and 3-9) (a), cpDNA(trnL-F and trn S-G) (b), and nrDNA (ITS, 15R-8, and Jr5680) (c). (PDF 449 kb)
11295_2017_1172_MOESM4_ESM.tif (95 kb)
Fig. S4Principal coordinate analyses (PCoA) of 108 individuals based on 11 microsatellite loci. Green Circle: Cluster I (J. regia), Red Circle: Cluster II (J. mandshurica), Purple Circle: Cluster III (J. hopeiensis). (GIF 24 kb)
11295_2017_1172_MOESM5_ESM.pdf (263 kb)
Fig. S5Isolation by distance (IBD) analysis of J. hopeiensis populations. The plot was generated using the allele data and geographic information from IBD. (PDF 262 kb)
11295_2017_1172_MOESM6_ESM.doc (46 kb)
Table S1(DOC 45 kb)
11295_2017_1172_MOESM7_ESM.doc (48 kb)
Table S2(DOC 48 kb)
11295_2017_1172_MOESM8_ESM.docx (37 kb)
Table S3(DOCX 36 kb)
11295_2017_1172_MOESM9_ESM.docx (20 kb)
Table S4(DOCX 19 kb)
11295_2017_1172_MOESM10_ESM.doc (42 kb)
Table S5(DOC 41 kb)
11295_2017_1172_MOESM11_ESM.xlsx (11 kb)
Table S6(XLSX 10 kb)
11295_2017_1172_MOESM12_ESM.xlsx (12 kb)
Table S7(XLSX 11 kb)

References

  1. Aradhya MK, Potter D, Gao F, Simon CJ (2007) Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective. Tree Genet Genomes 3:363–378CrossRefGoogle Scholar
  2. 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(3):892–901CrossRefPubMedGoogle Scholar
  3. Bai WN, Wang WT, Zhang DY (2014) Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree. Mol Phylogenet Evol 81:37–48CrossRefPubMedGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Bleeker W, Schmitz U, Ristow M (2007) Interspecific hybridisation between alien and native plant species in Germany and its consequences for native biodiversity. Biol Conserv 137:248–253CrossRefGoogle Scholar
  6. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154CrossRefPubMedGoogle Scholar
  7. Broadhurst LM, Lowe A, Coates DJ, Cunningham SA, McDonald M, Vesk PA, Yates C (2008) Seed supply for broadscale restoration: maximizing evolutionary potential. Evol Appl 1:587–597PubMedPubMedCentralGoogle Scholar
  8. Budd C, Zimmer E, Freeland JR (2015) Conservation genetics of Magnolia acuminata, an endangered species in Canada: can genetic diversity be maintained in fragmented, peripheral populations? Conserv Genet 16:1359–1373CrossRefGoogle Scholar
  9. Chen L, Ma Q, Chen Y, Wang B, Pei D (2014) Identification of major walnut cultivars grown in China based on nut phenotypes and SSR markers. Sci Hortic Amsterdam 168:240–248CrossRefGoogle Scholar
  10. Chen SL, Gilbert MG (2006) Flora of China. Science, Beijing and Missouri Botanical Garden Press, St LouisGoogle Scholar
  11. Crystal PA, Lichti NI, Woeste KE, Jacobs DF (2016) Vegetative and adaptive traits predict different outcomes for restoration using hybrids. Front Plant Sci 7:1741Google Scholar
  12. Dang M, Liu ZX, Chen X, Zhang T, Zhou HJ, Hu YH, Zhao P (2015) Identification, development, and application of 12 polymorphic EST-SSR markers for an endemic Chinese walnut (Juglans cathayensis L.) using next-generation sequencing technology. Biochem Syst Ecol 60:74–80CrossRefGoogle Scholar
  13. Dang M, Zhang T, Hu Y, Zhou H, Woeste KE, Zhao P (2016) De novo assembly and characterization of bud, leaf and flowers transcriptome from Juglans regia L. for the identification and characterization of new EST-SSRs. Forests 7:247CrossRefGoogle Scholar
  14. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  15. Dumolin-Lapegue S, Pemonge MH, Petit RJ (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6:393–397CrossRefPubMedGoogle Scholar
  16. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  17. Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  18. Ellstrand NC (1992) Gene flow by pollen: implications for plant conservation genetics. Oikos 63:77–86CrossRefGoogle Scholar
  19. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242Google Scholar
  20. 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
  21. Excoffier L (2007) ARLEQUIN, version 3.11. Computational and Molecular Population Genetics Lab, CMPG. Zoological Institute University of Berne, SwitzerlandGoogle Scholar
  22. 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 10:564–567CrossRefPubMedGoogle Scholar
  23. Fernández-Mazuecos M, Jiménez-Mejías P, Rotlan-Puig X, Vargas P (2014) Narrow endemics to Mediterranean islands: moderate genetic diversity but narrow climatic niche of the ancient, critically endangered Naufraga (Apiaceae). Perspect Plant Ecol 16:190–202CrossRefGoogle Scholar
  24. Fjellstrom RG, Parfitt DE (1995) Phylogenetic analysis and evolution of the genus Juglans (Juglandaceae) as determined from nuclear genome RFLPs. Plant Syst Evol 197:19–32CrossRefGoogle Scholar
  25. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedPubMedCentralGoogle Scholar
  26. Gómez JM, González-Megías A, Lorite J, Abdelaziz M, Perfectti F (2015) The silent extinction: climate change and the potential hybridization-mediated extinction of endemic high-mountain plants. Biodivers Conserv 24:1843–1857CrossRefGoogle Scholar
  27. Goto S, Iijima H, Ogawa H, Ohya K (2011) Outbreeding depression caused by intraspecific hybridization between local and nonlocal genotypes in Abies sachalinensis. Restor Ecol 19:243–250CrossRefGoogle Scholar
  28. Gunn BF, Aradhya M, Salick JM, Miller AJ, Yongping Y, Lin L, Xian H (2010) Genetic variation in walnuts (Juglans regia and J. sigillata; Juglandaceae): species distinctions, human impacts, and the conservation of agrobiodiversity in Yunnan, China. Am J Bot 97:660–671CrossRefPubMedGoogle Scholar
  29. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  30. Hao Y, Huang W, Wang K, Qi J, Xu J (2007) Analysis of Sect. Juglans germplasm in China using SSR marker. J Fruit Sci 5:012 (In Chinese) Google Scholar
  31. Hao YB, Wu CL, Chen YH, Dong NG, Wang WX, Qi JX, Pei D (2013) Selection of a new Juglans hopeiensis cultivar—‘Jingyi 1’. J Fruit Sci 30:718–719 (In Chinese) Google Scholar
  32. He N, Ning D, Xu T, Ma T, Li Y (2015) Early growth performance of introduction and cultivation of Juglans hopeiensis Hu in Yunnan province. For Invent Plan 40:106–109 (In Chinese) Google Scholar
  33. Hoban SM, Borkowski DS, Brosi SL, McCleary TIM, Thompson LM, McLachlan JS, Pereira M, Schlarbaum SE, Romero-Severson JEANNE (2010) Range-wide distribution of genetic diversity in the north American tree Juglans cinerea: a product of range shifts, not ecological marginality or recent population decline. Mol Ecol 19:4876–4891CrossRefPubMedGoogle Scholar
  34. Hoban SM, McCleary TS, Schlarbaum SE, Anagnostakis SL, Romero-Severson J (2012) Human-impacted landscapes facilitate hybridization between a native and an introduced tree. Evol Appl 5:720–731CrossRefPubMedPubMedCentralGoogle Scholar
  35. Holderegger R, Angelone S,·Brodbeck S,·Csencsics D,·Gugerli F,·Hoebee SE,·Finkeldey R (2005) Application of genetic markers to the discrimination of European black poplar (Populus nigra) from American black poplar (P. deltoides) and hybrid poplars (P. x canadensis) in Switzerland. Trees 19:742–747CrossRefGoogle Scholar
  36. Hu YH, Zhao P, Zhang Q, Wang Y, Gao XX, Zhang T, Zhou HJ, Dang M, Woeste KE (2015) De novo assembly and characterization of transcriptome using Illumina sequencing and development of twenty five microsatellite markers for an endemic tree Juglans hopeiensis Hu in China. Biochem Syst Ecol 63:201–211CrossRefGoogle Scholar
  37. Hu Z, Zhang T, Gao XX, Wang Y, Zhang Q, Zhou HJ, Zhao GF, Wang ML, Woeste KE, Zhao P (2016) De novo assembly and characterization of the leaf, bud, and fruit transcriptome from the vulnerable tree Juglans mandshurica for the development of 20 new microsatellite markers using Illumina sequencing. Mol Gen Genomics 291:849–862CrossRefGoogle Scholar
  38. Hu YH, Woeste KE, Zhao P (2017) Completion of the chloroplast genomes of five Chinese Juglans and their contribution to chloroplast phylogeny. Front Plant Sci 7:1955CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jensen J, Bohonak AJ, Kelley SK (2005) Isolation by distance Web service. BMC Genet 6:13CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  41. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  42. Kimura M, Seiwa K, Suyama Y, Ueno N (2003) Flowering system of heterodichogamous Juglans ailanthifolia. Plant Spec Biol 18:75–84CrossRefGoogle Scholar
  43. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  44. Lu AM (1982) The geographical dispersal of Juglandaceae. Acta Phytotaxon Sin 20:257–274Google Scholar
  45. Lu AM, Stone DE, Grauke LJ (1999) Juglandaceae. Flora China 4:277–285Google Scholar
  46. Manning WE (1978) The classification within the Juglandaceae. Ann Mo Bot Gard 65:1058–1087CrossRefGoogle Scholar
  47. Matthies D, Bräuer I, Maibom W, Tscharntke T (2004) Population size and the risk of local extinction: empirical evidence from rare plants. Oikos 105:481–488CrossRefGoogle Scholar
  48. McGranahan G, Leslie C (1991) Walnuts (Juglans). Genet Resour Temp Fruit Nut Crops 290:907–974Google Scholar
  49. Millar MA, Byrne M, Nuberg IK, Sedgley M (2012) High levels of genetic contamination in remnant populations of Acacia saligna from a genetically divergent planted stand. Restor Ecol 20:260–267CrossRefGoogle Scholar
  50. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254CrossRefPubMedGoogle Scholar
  51. Mousset S, Derome N, Veuille M (2004) A test of neutrality and constant population size based on the mismatch distribution. Mol Biol Evol 21:724–731CrossRefPubMedGoogle Scholar
  52. Mu YL, Xi RT, Lu ZR (1990) Microsporogenesis observation and karyotype analysis of some species in genus Juglans L. J Wuhan Bot Res 3:301–310 (In Chinese) Google Scholar
  53. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pei D, Li R, Liu Z, Wang F (2006) Conservation, exploration and utilization of Juglans hopeiensis Hu resources. For Resour Manag 4:66–69 (In Chinese) Google Scholar
  55. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. J Hered 90:502–503CrossRefGoogle Scholar
  56. Pollegioni P, Woeste K, Olimpieri I, Marandola D, Cannata F, Malvolti ME (2011) Long-term human impacts on genetic structure of Italian walnut inferred by SSR markers. Tree Genet Genomes 7:707–723CrossRefGoogle Scholar
  57. Pollegioni P, Woeste KE, Chiocchini F, Del Lungo S, Olimpieri I, Tortolano V, Clark J, Hemery GE, Mapelli S, Malvolti ME (2015) Ancient humans influenced the current spatial genetic structure of common walnut populations in Asia. PLoS One 10:e0135980CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pollegioni P, Woeste K, Chiocchini F, Del Lungo S, Ciolfi M, Olimpieri I, Tortolano V, Clark J, Hemery GE, Mapelli S, Malvolti ME (2017) Rethinking the history of common walnut (Juglans regia L.) in Europe: its origins and human interactions. PloS ONE 12:e0172541CrossRefPubMedPubMedCentralGoogle Scholar
  59. Poudel RC, Möller M, Li DZ, Shah A, Gao LM (2014) Genetic diversity, demographical history and conservation aspects of the endangered yew tree Taxus contorta (syn. Taxus fuana) in Pakistan. Tree Genet Genomes 10:653–665CrossRefGoogle Scholar
  60. Pouget M, Youssef S, Migliore J, Juin M, Médail F, Baumel A (2013) Phylogeography sheds light on the central–marginal hypothesis in a Mediterranean narrow endemic plant. Ann Bot 112(7):1409–1420CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  62. Raymond M, Rousset F (1995) GENEPOP, version 1.2: polulation genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  63. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  64. Ruan Y, Huang BH, Lai SJ, Wan YT, Li JQ, Huang S, Liao PC (2013) Population genetic structure, local adaptation, and conservation genetics of Kandelia obovata. Tree Genet Genomes 9:913–925CrossRefGoogle Scholar
  65. Shu Z, Zhang X, Yu D, Xue S, Wang H (2016) Natural hybridization between Persian walnut and Chinese walnut revealed by simple sequence repeat markers. J Am Soc Sci 141:146–150Google Scholar
  66. Stanford AM, Harden R, Parks CR (2000) Phylogeny and biogeography of Juglans (Juglandaceae) based on matK and ITS sequence data. Am J Bot 87:872–882CrossRefPubMedGoogle Scholar
  67. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefPubMedPubMedCentralGoogle Scholar
  68. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  69. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting and genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  70. Victory ER, Glaubitz JC, Rhodes OE Jr, Woeste KE (2006) Genetic homogeneity in Juglans nigra (Juglandaceae) at nuclear microsatellites. Am J Bot 93:118–126CrossRefGoogle Scholar
  71. Vilà M, Weber E, Antonio CM (2000) Conservation implications of invasion by plant hybridization. Biol Invasions 2:207–217CrossRefGoogle Scholar
  72. Wang H, Zhang Z, Wang W, Gao Y, Sun H (2005) Studies on photosynthetic characteristics of Juglans hopeiensis Hu in the field. Actahorticulturae Sin 32:392–396 (In Chinese) Google Scholar
  73. Wang H, Pan G, Ma Q, Zhang J, Pei D (2015) The genetic diversity and introgression of Juglans regia and Juglans sigillata in Tibet as revealed by SSR markers. Tree Genet Genomes 11:1–11CrossRefGoogle Scholar
  74. Wang WT, Xu B, Zhang DY, Bai WN (2016) Phylogeography of postglacial range expansion in Juglans mandshurica (Juglandaceae) reveals no evidence of bottleneck, loss of genetic diversity, or isolation by distance in the leading-edge populations. Mol Phylogenet Evol 102:255–264CrossRefPubMedGoogle Scholar
  75. Wu Y, Pei D, Xi K (1999) Analysis of the origin and the taxonomic position of Juglans hopeiensis using RAPD markers. Sci Silvae Sin 35:25–30 (In Chinese) Google Scholar
  76. Xi RT (1990) Discussion on the origin of walnut in china. Acta Horticulturae (In Chinese)Google Scholar
  77. Zhang JT, Shao D (2015) Attributes of forest diversity in the Yunmeng Mountain National Forest Park in Beijing, China. Appl Ecol Environ Res 13:769–782Google Scholar
  78. Zhang Q, Chiang TY, George M, Liu JQ, Abbott RJ (2005) Phylogeography of the Qinghai-Tibetan Plateau endemic Juniperus przewalskii (Cupressaceae) inferred from chloroplast DNA sequence variation. Mol Ecol 14:3513–3524CrossRefPubMedGoogle Scholar
  79. Zhao P, Woeste KE (2011) DNA markers identify hybrids between butternut (Juglans cinerea L.), and Japanese walnut (Juglans ailantifolia Carr.) Tree Genet Genomes 7:511–533CrossRefGoogle Scholar
  80. Zhao P, Zhou HJ, Liu ZL, Woeste KE, Hu DF, Dang M, Li ZH, Wang ML, Zhao GF (2014) A review of research progress on molecular phylogeny and biogeography in Juglans. Sci Silvae Sin 50:147–157 (In Chinese) Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life SciencesNorthwest UniversityXi’anChina
  2. 2.USDA Forest Service Hardwood Tree Improvement and Regeneration Center (HTIRC), Department of Forestry and Natural ResourcesPurdue UniversityWest LafayetteUSA

Personalised recommendations