Advertisement

Tree Genetics & Genomes

, 14:48 | Cite as

The southwestern origin and eastward dispersal of pear (Pyrus pyrifolia) in East Asia revealed by comprehensive genetic structure analysis with SSR markers

  • Lei Xue
  • Qingwen Liu
  • Hongju Hu
  • Yue Song
  • Jing Fan
  • Bing Bai
  • Mingyue Zhang
  • Runze Wang
  • Mengfan Qin
  • Xiaolong Li
  • Jun Wu
Original Article
  • 132 Downloads
Part of the following topical collections:
  1. Germplasm Diversity

Abstract

Pyrus pyrifolia is considered one of the most important cultivated Pyrus species. Hundreds of landraces and bred cultivars have been developed through the natural and artificial hybridizations necessary due to self-incompatibility. In this study, the genetic diversity of 478 Pyrus accessions, including Chinese landraces, bred cultivars, and wild samples, as well as introduced pear cultivars from Japan and Korea, was investigated with a set of 17 simple sequence repeat (SSR) markers distributed across all 17 linkage groups of the pear genome. A total of 121 alleles were detected, including 4 rare alleles with a frequency lower than 5%. Diversity statistics indicated a high level of genetic variation as quantified by the average values of the observed heterozygosity, the expected heterozygosity, and Wright’s fixation index, at 0.76, 0.78, and 0.02, respectively. Population structure and discriminant analysis of principal component analysis implied extensive genetic communication between sand pears in China and revealed four contiguous geographical clusters with overlapping geographical regions. The diversity of the four clusters and approximate Bayesian computation (ABC) indicated that sand pear spread from west to east along the Pearl River and Yangtze River valleys. High diversity and polyphyletic genetic components of cultivars in southwestern China further support southwestern China as the probable center of divergence for Pyrus species. A core collection of 80 out of 470 cultivars was selected, accounting for about 17% of accessions, and capturing 91% of all alleles, including all rare alleles. Our research provides a comprehensive understanding of sand pear germplasm in East Asia and constructs a preliminary core collection, which will be useful for association genetics studies, germplasm conservation, and breeding programs.

Keywords

Sand pear (Pyrus pyrifoliaGenetic diversity Population structure Migration route Core collection 

Notes

Funding information

This work was financially supported by the National Science Foundation of China (31672111), the Earmarked Fund for China Agriculture Research System (CARS-29), the Science Foundation for Distinguished Young Scientists in Jiangsu Province (BK20150025), and The Six Talent Peaks Project in Jiangsu Province (2014-NY-025).

Supplementary material

11295_2018_1255_MOESM1_ESM.pdf (122 kb)
Fig. S1 Distribution of pairwise relatedness coefficients among the P. pyrifolia individuals. rxy values among cultivars are normally distributed around a mean of zero, with a low variance between pairs of individuals. (PDF 121 kb)
11295_2018_1255_MOESM2_ESM.jpg (171 kb)
Fig. S2 Modeling of number of genepools in P. pyrifolia using STRUCTURE. Ln P(D) and delta K, calculated according to Evanno et al. (2005), plotted against the number of modeled genepools (K). (JPG 170 kb)
11295_2018_1255_MOESM3_ESM.pdf (310 kb)
Fig. S3 Inference of the number of clusters. Bayesian information criterion (BIC) is provided for different numbers of clusters (from 1 to 50). The chosen number of clusters (8) is crossed in black. (PDF 310 kb)
11295_2018_1255_MOESM4_ESM.pdf (369 kb)
Fig. S4 Scatterplots of DAPC. Groups are shown by different colors and inertia ellipses; dots represent individual strains. (PDF 368 kb)
11295_2018_1255_MOESM5_ESM.docx (39 kb)
ESM 1 (DOCX 38.6 kb)
11295_2018_1255_MOESM6_ESM.docx (14 kb)
ESM 2 (DOCX 13.7 kb)
11295_2018_1255_MOESM7_ESM.docx (18 kb)
ESM 3 (DOCX 17.6 kb)

References

  1. Aranzana MJ, Abbassi E, Howad W, Arús P (2010) Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet 11(1):69CrossRefPubMedPubMedCentralGoogle Scholar
  2. Balas FC, Osuna MD, Domínguez G, Pérez-Gragera F, López-Corrales M (2014) Ex situ conservation of underutilised fruit tree species: establishment of a core collection for Ficus carica L. using microsatellite markers (SSRs). Tree Genet Genomes 10:703–710CrossRefGoogle Scholar
  3. Baraket G, Chatti K, Saddoud O, Abdelkarim AB, Mars M, Trifi M, Hannachi AS (2011) Comparative assessment of SSR and AFLP markers for evaluation of genetic diversity and conservation of fig, Ficus carica L., genetic resources in Tunisia. Plant Mol Biol Report 29:171–184CrossRefGoogle Scholar
  4. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025PubMedPubMedCentralGoogle Scholar
  5. Brown A (1989) Core collections: a practical approach to genetic resources management. Genome 31:818–824CrossRefGoogle Scholar
  6. Brown. A., Marshall, DR. (1973) Optimum sampling strategies in genetic conservation (summary). Lecture Notes in Computer Science  4768:36–56Google Scholar
  7. Campbell CS, Evans RC, Morgan DR, Dickinson TA, Arsenault MP (2007) Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Syst Evol 266:119–145CrossRefGoogle Scholar
  8. Campoy JA, Ruiz D, Egea J, Rees DJG, Celton JM, Martínez-Gómez P (2011) Inheritance of flowering time in apricot (Prunus armeniaca L.) and analysis of linked quantitative trait loci (QTLs) using simple sequence repeat (SSR) markers. Plant Mol Biol Report 29:404–410CrossRefGoogle Scholar
  9. Challice JS, Westwood MN (1973) Numerical taxonomic studies of the genus Pyrus using both chemical and botanical characters. Bot J Linn Soc 67:121–148CrossRefGoogle Scholar
  10. Chen H, Song Y, Li L, Khan MA, Li X, Korban SS, Wu J, Zhang S (2015) Construction of a high-density simple sequence repeat consensus genetic map for pear (Pyrus spp.). Plant Mol Biol Report 33:316–325CrossRefGoogle Scholar
  11. Cornuet (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11:401CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dong D, Fu X, Yuan F, Chen P, Zhu S, Li B, Yang Q, Yu X, Zhu D (2014) Genetic diversity and population structure of vegetable soybean (Glycine max (L.) Merr.) in China as revealed by SSR markers. Genet Resour Crop Evol 61:173–183CrossRefGoogle Scholar
  14. Dos Santos ARF, Ramos-Cabrer AM, Díaz-Hernández MB, Pereira-Lorenzo S (2011) Genetic variability and diversification process in local pear cultivars from northwestern Spain using microsatellites. Tree Genet Genomes 7:1041–1056CrossRefGoogle Scholar
  15. 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
  16. Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13(1):39CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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
  18. Fagundes NJR, Ray N, Beaumont M, Neuenschwander S, Salzano FM, Bonatto SL, Excoffier L (2007) Statistical evaluation of alternative models of human evolution. Proceedings of the National Academy of Sciences 104(45):17614–17619.CrossRefGoogle Scholar
  19. 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
  20. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fan L, Zhang M, Liu Q, Li L, Song Y, Wang L, Zhang S, Wu J (2013) Transferability of newly developed pear SSR markers to other Rosaceae species. Plant Mol Biol Report 31:1271–1282CrossRefPubMedPubMedCentralGoogle Scholar
  22. Franco J, Crossa J, Taba S, Shands H (2005) A sampling strategy for conserving genetic diversity when forming core subsets. Crop Sci 45:1035–1044CrossRefGoogle Scholar
  23. Hamrick JL, Godt M (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society B-Biological Sciences 351:1291–1298CrossRefGoogle Scholar
  24. Hoelzel AR (2010) Looking backwards to look forwards: conservation genetics in a changing world. Conserv Genet 11:655–660CrossRefGoogle Scholar
  25. Hokanson SC, Lamboy WF, Szewc-McFadden AK, McFerson JR (2001) Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids. Euphytica 118:281–294CrossRefGoogle Scholar
  26. Hu J, Wang P, Su Y, Wang R, Li Q, Sun K (2015) Microsatellite diversity, population structure, and core collection formation in melon germplasm. Plant Mol Biol Report 33:439–447CrossRefGoogle Scholar
  27. Jiang S, Zong Y, Yue X, Postman J, Teng Y, Cai D (2015) Prediction of retrotransposons and assessment of genetic variability based on developed retrotransposon-based insertion polymorphism (RBIP) markers in Pyrus L. Mol Gen Genomics 290:225–237CrossRefGoogle Scholar
  28. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  29. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kim K, Chung H, Cho G, Ma K, Chandrabalan D, Gwag J, Kim T, Cho E, Park Y (2007) PowerCore: a program applying the advanced M strategy with a heuristic search for establishing core sets. Bioinformatics 23:2155–2162CrossRefPubMedGoogle Scholar
  31. Lassois L, Denancé C, Ravon E, Guyader A, Guisnel R, Hibrand-Saint-Oyant L, Poncet C, Lasserre-Zuber P, Feugey L, Durel C (2016) Genetic diversity, population structure, parentage analysis, and construction of core collections in the French apple germplasm based on SSR markers. Plant Mol Biol Report 34:827–844CrossRefGoogle Scholar
  32. Le Cunff L, Fournier-Level A, Laucou V, Vezzulli S, Lacombe T, Adam-Blondon A, Boursiquot J, This P (2008) Construction of nested genetic core collections to optimize the exploitation of natural diversity in Vitis vinifera L. subsp. sativa. BMC Plant Biol 8(1):31CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lin Z, Zhang X, Nie Y, He D, Wu M (2003) Construction of a genetic linkage map for cotton based on SRAP. Chin Sci Bull 48:2064–2068CrossRefGoogle Scholar
  34. Liu J, Zheng X, Potter D, Hu C, Teng Y (2012) Genetic diversity and population structure of Pyrus calleryana (Rosaceae) in Zhejiang province, China. Biochem Syst Ecol 45:69–78CrossRefGoogle Scholar
  35. Liu J, Sun P, Zheng X, Potter D, Li K, Hu C, Teng Y (2013) Genetic structure and phylogeography of Pyrus pashia L. (Rosaceae) in Yunnan Province, China, revealed by chloroplast DNA analyses. Tree Genet Genomes 9:433–441CrossRefGoogle Scholar
  36. Liu QW, Song Y, Liu L, Zhang MY, Sun JM, Zhang SL, Wu J (2015) Genetic diversity and population structure of pear (Pyrus spp.) collections revealed by a set of core genome-wide SSR markers. Tree Genetics & Genomes 11(6):1–22Google Scholar
  37. Lo EY, Stefanović S, Christensen KI, Dickinson TA (2009) Evidence for genetic association between East Asian and western North American Crataegus L. (Rosaceae) and rapid divergence of the eastern North American lineages based on multiple DNA sequences. Mol Phylogenet Evol 51:157–168CrossRefPubMedGoogle Scholar
  38. Lombard, P.B., Westwood, M.N., 1987. Pear rootstocksGoogle Scholar
  39. Lu J, Wu J, Zhang S, Wu H, Zhang Y (2011) Genetic diversity and polygentic relationship among pears reveled by SSR analysis. Journal of Nanjing Agricultural University 2:009Google Scholar
  40. Newton AC, Allnutt TR, Gillies A, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol 14:140–145CrossRefPubMedGoogle Scholar
  41. Odong TL, Jansen J, Van Eeuwijk FA, van Hintum TJ (2013) Quality of core collections for effective utilisation of genetic resources review, discussion and interpretation. Theor Appl Genet 126:289–305CrossRefPubMedGoogle Scholar
  42. 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
  43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  44. Pu F, Wang Y (1963) Pomology of China. Pears. Shanghai Scientific and Technical Publishers, Shanghai (in Chinese) Google Scholar
  45. Richards CM, Volk GM, Reilley AA, Henk AD, Lockwood DR, Reeves PA, Forsline PL (2009) Genetic diversity and population structure in Malus sieversii, a wild progenitor species of domesticated apple. Tree Genet Genomes 5:339–347CrossRefGoogle Scholar
  46. Rubtsov GA (1944) Geographical distribution of the genus Pyrus and trends and factors in its evolution. Am Nat 78:358–366CrossRefGoogle Scholar
  47. Schoen DJ, Brown AH (1993) Conservation of allelic richness in wild crop relatives is aided by assessment of genetic markers. Proc Natl Acad Sci 90:10623–10627CrossRefPubMedGoogle Scholar
  48. Shen D, Bo W, Xu F, Wu R (2014) Genetic diversity and population structure of the Tibetan poplar (Populus szechuanica var. tibetica) along an altitude gradient. BMC Genet 15:1CrossRefGoogle Scholar
  49. Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65CrossRefPubMedGoogle Scholar
  50. Song Y, Fan L, Chen H, Zhang M, Ma Q, Zhang S, Wu J (2014) Identifying genetic diversity and a preliminary core collection of Pyrus pyrifolia cultivars by a genome-wide set of SSR markers. Sci Hortic 167:5–16CrossRefGoogle Scholar
  51. Taberlet P, Fumagalli L, Wustsaucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464CrossRefPubMedGoogle Scholar
  52. Tautz D (1989) Hypervariabflity of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471CrossRefPubMedPubMedCentralGoogle Scholar
  53. Teng Y, Tanabe K, Tamura F, Itai A (2002) Assessment of genetic relatedness among large-fruited pear cultivars native to east asia using rapd markers. Acta Horticulturae (587):139–145Google Scholar
  54. Vargas AM, de Andrés MT, Ibáñez J (2016) Maximization of minority classes in core collections designed for association studies. Tree Genet Genomes 12Google Scholar
  55. Vercken E, Fontaine MC, Gladieux P, Hood ME, Jonot O, Giraud T (2010) Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathog 6:e1001229CrossRefPubMedPubMedCentralGoogle Scholar
  56. Wu J, Li L, Li M, Khan MA, Li X, Chen H, Yin H, Zhang S (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. Journal of Experimental Botany 65(20):5771–5781Google Scholar
  57. Wuyun T, Amo H, Xu J, Ma T, Uematsu C, Katayama H (2015) Population structure of and conservation strategies for wild Pyrus ussuriensis Maxim. in China. PLoS One 10:e0133686CrossRefPubMedPubMedCentralGoogle Scholar
  58. Yeh FC, Yang R, Boyle TB, Ye ZH, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular biology and biotechnology centre. University of Alberta, Canada, p 10Google Scholar
  59. Yu (1979a) Taxonomy of the fruit tree in China (in Chinese). Beijing, China Agr PressGoogle Scholar
  60. Yu DJ (1979b) Pyrus pyrifolia. Flora Republicae Popularis Sinicae 36:365Google Scholar
  61. Zhang P, Li J, Li X, Liu X, Zhao X, Lu Y (2011) Population structure and genetic diversity in a rice core collection (Oryza sativa L.) investigated with SSR markers. PLoS One 6:e27565CrossRefPubMedPubMedCentralGoogle Scholar
  62. Zhang MY, Fan L, Liu QZ, Song Y, Wei SW (2014) A novel set of EST-derived SSR markers for pear and cross-species transferability in Rosaceae. Plant Mol Biol Report 32:290-302Google Scholar
  63. Zheng X, Cai D, Potter D, Postman J, Liu J, Teng Y (2014) Phylogeny and evolutionary histories of Pyrus L. revealed by phylogenetic trees and networks based on data from multiple DNA sequences. Mol Phylogenet Evol 80:54–65CrossRefPubMedGoogle Scholar
  64. Zong Y, Sun P, Liu J, Yue X, Niu Q, Teng Y (2014) Chloroplast DNA-based genetic diversity and phylogeography of Pyrus betulaefolia (Rosaceae) in northern China. Tree Genet Genomes 10:739–749CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lei Xue
    • 1
  • Qingwen Liu
    • 1
  • Hongju Hu
    • 2
  • Yue Song
    • 1
  • Jing Fan
    • 2
  • Bing Bai
    • 1
  • Mingyue Zhang
    • 1
  • Runze Wang
    • 1
  • Mengfan Qin
    • 1
  • Xiaolong Li
    • 1
  • Jun Wu
    • 1
  1. 1.Center of Pear Engineering Technology Research, State Key Laboratory of Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanjingChina
  2. 2.Research Institute of Fruit and TeaHubei Academy of Agricultural ScienceWuhanChina

Personalised recommendations