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Plant Molecular Biology Reporter

, Volume 37, Issue 1–2, pp 63–73 | Cite as

Application of High-Throughput Sequencing to Evaluate the Genetic Diversity Among Wild Apple Species Indigenous to Shandong, China, and Introduced Cultivars

  • Yuansheng Chang
  • Ping He
  • Haibo Wang
  • Huifeng Li
  • Sen Wang
  • Linguang LiEmail author
Original Paper
  • 232 Downloads

Abstract

The Taiyi mountainous region of Shandong province in eastern China has an abundance of wild Malus species. We evaluated the genetic diversity of 88 Malus accessions (45 Asian apple cultivars, 10 American apple cultivars, 12 European apple cultivars, 19 Chinese wild apples, and two apple cultivars with unknown origins) based on single-nucleotide polymorphism (SNP) markers. A total of 38,364 SNPs were obtained with an average of 2256 SNPs per chromosome. The average of the polymorphism information content (PIC), gene diversity, and allele frequency for SNPs was 0.268, 0.306, and 0.364, respectively. A circular phylogenetic tree constructed based on SNP data revealed that the 88 Malus accessions could be divided into three groups. However, a population structure analysis suggested the 88 Malus accessions could be divided into four groups. A principal component analysis (PCA) revealed some population stratification. The first three PCs accounted for 41.62% of the population-wide SNP variation, with PC1 accounting for 33.9%. Moreover, the kinship values of the 88 Malus accessions ranged from 0 to 2.36, with 96.42% of the kinship values between 0 and 0.2. A phylogenetic tree and a PCA indicated the Chinese wild apples widely distributed among the cultivated apples had a diverse genetic background. Characterizing the genetic relationships between cultivated apples and Chinese wild apples is essential for increasing the genetic diversity of the germplasms used by apple breeders.

Keywords

Malus Genetic diversity SLAF-seq Cluster analysis 

Notes

Acknowledgments

We would like to thank China agriculture scientific research institutions and agriculture university supplying the experimental materials. We also would like to thank Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

Funding Information

This project was supported by the Youth Fund for Shandong Academy of Agriculture Sciences (2016YQN30), the Agricultural Innovation Project for Shandong Academy of Agriculture Sciences (CXGC2016B07), and the Earmarked Fund for China Agriculture Research System (CARS-28).

Supplementary material

11105_2019_1138_MOESM1_ESM.xlsx (62 kb)
ESM 1 (XLSX 62 kb)

References

  1. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655–1664 http://www.genome.org/cgi/doi/10.1101/gr.094052.109. Accessed 18 Apr 2018
  2. Amyotte B, Bowen AJ, Banks T, Rajcan I, Somers DJ (2017) Mapping the sensory perception of apple using descriptive sensory evaluation in a genome wide association study. PLoS One 12(2):e0171710.  https://doi.org/10.1371/journal.pone.0171710 CrossRefGoogle Scholar
  3. Bianco L, Cestaro A, Sargent DJ, Banchi E, Derdak S, Di Guardo M, Salvi S, Jansen J, Viola R, Gut L, Laurens F, Chagné D, Velasco R, van de Weg E, Troggio M (2014) Development and validation of a 20K single nucleotide polymorphism (SNP) whole genome genotyping array for apple (Malus × domestica Borkh). PLoS One 9(10):e110377.  https://doi.org/10.1371/journal.pone.0110377 CrossRefGoogle Scholar
  4. Bianco L, Cestaro A, Linsmith G, Muranty H, Denancé C, Théron A, Poncet C, Micheletti D, Kerschbamer E, Di Pierro EA, Larger S, Pindo M, Van de Weg E, Davassi A, Laurens F, Velasco R, Durel C, Troggio M (2016) Development and validation of the Axiom®Apple 480K SNP genotyping array. Plant J 86:62–74.  https://doi.org/10.1111/tpj.13145 CrossRefGoogle Scholar
  5. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32(3):314–331Google Scholar
  6. Chagné D, Crowhurst RN, Troggio M, Davey MW, Gilmore B, Lawley C, Vanderzande S, Hellens RP, Kumar S, Cestaro A, Velasco R, Main D, Rees JD, Iezzoni A, Mockler T, Wilhelm L, Van de Weg E, Gardiner SE, Bassil N, Peace C (2012) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One 7(2):e31745.  https://doi.org/10.1371/journal.pone.0031745 CrossRefGoogle Scholar
  7. Clark MD, Schmitz CA, Rosyara UR, Luby JJ, Bradeen JM (2014) A consensus ‘Honeycrisp’ apple (Malus × domestica) genetic linkage map from three full-sib progeny populations. Tree Genet Genomes 10:627–639.  https://doi.org/10.1007/s11295-014-0709-1 CrossRefGoogle Scholar
  8. Coart E, Vekemans X, Smulders MJM, Wagner I, Van Huylenbroeck J, Van Bockstaele E, Roldán-Ruiz I (2003) Genetic variation in the endangered wild apple (Malus sylvestris (L.) Mill.) in Belgium as revealed by amplified fragment length polymorphism and microsatellite markers. Mol Ecol 12:845–857.  https://doi.org/10.1046/j.1365-294X.2003.01778.x CrossRefGoogle Scholar
  9. Cornille A, Giraud T, Smulders MJM, Roldán-Ruiz I, Gladieux P (2014) The domestication and evolutionary ecology of apples. Trends Genet 30:57–65.  https://doi.org/10.1016/j.tig.2013.10.002 CrossRefGoogle Scholar
  10. Di Guardo M, Bink MCAM, Guerra W, Letschka T, Lozano L, Busatto N, Poles L, Tadiello A, Bianco L, Visser RGF, van de Weg E, Costa E (2017) Deciphering the genetic control of fruit texture in apple by multiple family-based analysis and genome-wide association. J Exp Bot 68(7):1451–1466.  https://doi.org/10.1093/jxb/erx017 CrossRefGoogle Scholar
  11. Di Pierro EA, Gianfranceschi L, Guardo MD, Putten HJJK, Kruisselbrink JW, Longhi S, Troggio M, Bianco L, Muranty H, Pagliarani G, Tartarini S, Letschka T, Luis LL, Garkava-Gustavsson L, Micheletti D, Bink MCAM, Voorrips RE, Aziz E, Velasco R, Laurens F, Van de Weg WE (2016) A high-density, multi-parental SNP genetic map on apple validates a new mapping approach for outcrossing species. Hortic Res 3:16057.  https://doi.org/10.1038/hortres.2016.57 CrossRefGoogle Scholar
  12. Duan N, Bai Y, Sun H, Wang N, Ma Y, Li M, Wang X, Jiao C, Legall N, Mao L, Wan S, Wang K, He T, Feng S, Zhang Z, Mao Z, Shen X, Chen X, Jiang Y, Wu S, Yin C, Ge S, Yang L, Jiang S, Xu H, Liu J, Wang D, Qu C, Wang Y, Zuo W, Xiang L, Liu C, Zhang D, Gao Y, Xu Y, Xu K, Chao T, Fazio G, Shu H, Zhong G, Cheng L, Fei Z, Chen X (2017) Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun 8:249.  https://doi.org/10.1038/s41467-017-00336-7 CrossRefGoogle Scholar
  13. Dunemann F, Kahnau R, Schmidt H (1994) Genetic relationships in Malus evaluated by RAPD ‘fingerprinting’ of cultivars and wild species. Plant Breed 113:150–159  https://doi.org/10.1111/j.1439-0523.1994.tb00717.x CrossRefGoogle Scholar
  14. Farneti B, Di Guardo M, Khomenko I, Cappellin L, Biasioli F, Velasco R, Costa F (2017) Genome-wide association study unravels the genetic control of the apple volatilome and its interplay with fruit texture. J Exp Bot 68(7):1467–1478.  https://doi.org/10.1093/jxb/erx018 CrossRefGoogle Scholar
  15. Ferreira V, Ramos-Cabrer AM, Carnide V, Pinto-Carnide O, Assunção A, Marreiros A, Rodrigues R, Pereira-Lorenzo S, Castro I (2016) Genetic pool structure of local apple cultivars from Portugal assessed by microsatellites. Tree Genet Genomes 12:36.  https://doi.org/10.1007/s11295-016-0997-8 CrossRefGoogle Scholar
  16. Galli Z, Halász G, Kiss E, Heszky L, Dobránszki J (2005) Molecular identification of commercial apple cultivars with microsatellite markers. HortSci 40:1974–1977CrossRefGoogle Scholar
  17. Gardner KM, Brown P, Cooke TF, Cann S, Costa F, Bustamante C, Velasco R, Troggio M, Myles S (2014) Fast and cost-effective genetic mapping in apple using next-generation sequencing. G3-Genes Genom Genet 4:1681–1687.  https://doi.org/10.1534/g3.114.011023 Google Scholar
  18. Goulão L, Oliveira CM (2001) Molecular characterisation of cultivars of apple (Malus × domestica Borkh.) using microsatellite (SSR and ISSR) markers. Euphytica 122:81–89.  https://doi.org/10.1023/A:1012691814643 CrossRefGoogle Scholar
  19. Goulão L, Cabrita L, Oliveira CM, Leitão JM (2001) Comparing RAPD and AFLP™ analysis in discrimination and estimation of genetic similarities among apple (Malus domestica Borkh.) cultivars. Euphytica 119:259–270CrossRefGoogle Scholar
  20. Hardy QJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620.  https://doi.org/10.1046/j.1471-8286.2002.00305.x CrossRefGoogle Scholar
  21. Höfer M, Ali MAMSE, Sellmann J, Peil A (2014) Phenotypic evaluation and characterization of a collection of Malus species. Genet Resour Crop Evol 61:943–964.  https://doi.org/10.1007/s10722-014-0088-3 CrossRefGoogle Scholar
  22. Howard NP, Van De Weg E, Bedford DS, Peace CP, Vanderzande S, Clark MD, Luby JJ (2017) Elucidation of the ‘Honeycrisp’pedigree through haplotype analysis with a multi-family integrated SNP linkage map and a large apple (Malus × domestica) pedigree-connected SNP data set. Hortic Res 4:17003CrossRefGoogle Scholar
  23. Howard NP, van de Weg E, Tillman J, Tong CB, Silverstein KA, Luby JJ (2018) Two QTL characterized for soft scald and soggy breakdown in apple (Malus × domestica) through pedigree-based analysis of a large population of interconnected families. Tree Genet Genomes 14(1):2.  https://doi.org/10.1007/s11295-017-1216-y CrossRefGoogle Scholar
  24. Janisiewicz WJ, Saftner RA, Conway WS, Forsline PL (2008) Preliminary evaluation of apple germplasm from Kazakhstan for resistance to postharvest blue mold in fruit caused by Penicillium expansum. HortSci 43:420–426CrossRefGoogle Scholar
  25. Kellerhals M, Bertschinger L, Gessler C (2004) Use of genetic resources in apple breeding and for sustainable fruit production. J Fruit Ornam Plant Res 12:53–62 (Special)Google Scholar
  26. Koller B, Lehmann A, McDermott JM, Gessler C (1993) Identification of apple cultivars using RAPD markers. Theor Appl Genet 85:901–904CrossRefGoogle Scholar
  27. Kumar S, Volz R, Alspach P, Bus V (2010) Development of a recurrent apple breeding programme in New Zealand: a synthesis of results, and a proposed revised breeding strategy. Euphytica 173:207–222.  https://doi.org/10.1007/s10681-009-0090-6 CrossRefGoogle Scholar
  28. Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C, Carlisle C (2012) Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.). PLoS One 7(5):e36674.  https://doi.org/10.1371/journal.pone.0036674 CrossRefGoogle Scholar
  29. Larsen B, Toldam-Andersen TB, Pedersen C, Ørgaard M (2017) Unravelling genetic diversity and cultivar parentage in the Danish apple gene bank collection. Tree Genet Genomes 13:14.  https://doi.org/10.1007/s11295-016-1087-7 CrossRefGoogle Scholar
  30. Lassois L, Denancé C, Ravon E, Guyader A, Guisnel R, Hibrand-Saint-Oyant L, Poncet C, Lasserre-Zuber P, Feugey L, Durel CE (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 34:827–844.  https://doi.org/10.1007/s11105-015-0966-7 CrossRefGoogle Scholar
  31. Laurens F, Durel CE, Lascostes M (2004) Molecular characterization of French local apple cultivars using SSRs. XI Eucarpia Symposium on Fruit Breeding and Genetics 663:639–642.  https://doi.org/10.17660/ActaHortic.2004.663.114
  32. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefGoogle Scholar
  33. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) 1000 genome project data processing subgroup. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079.  https://doi.org/10.1093/bioinformatics/btp352 CrossRefGoogle Scholar
  34. Li Z, Zuo LH, Yang MS, Zhang J (2017) Genetic diversity analysis of three apple populations by SSR markers. J Agr U Hebei 4(40):50–56Google Scholar
  35. Liang W, Dondini L, De Franceschi P, Paris R, Sansavini S, Tartarini S (2015) Genetic diversity, population structure and construction of a core collection of apple cultivars from Italian germplasm. Plant Mol Biol Report 33:458–473.  https://doi.org/10.1007/s11105-014-0754-9 CrossRefGoogle Scholar
  36. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129.  https://doi.org/10.1093/bioinformatics/bti282 CrossRefGoogle Scholar
  37. Maguire TL, Collins GG, Sedgley M (1994) A modified CTAB DNA extraction procedure for plants belonging to the family Proteaceae. Plant Mol Biol Report 12:106–109CrossRefGoogle Scholar
  38. Marconi G, Ferradini N, Russi L, Concezzi L, Veronesi F, Albertini E (2018) Genetic characterization of the apple germplasm collection in Central Italy: the value of local varieties. Front Plant Sci 9:1460.  https://doi.org/10.3389/fpls.2018.01460 CrossRefGoogle Scholar
  39. McClure KA, Gardner KM, Toivonen PMA, Hampson CR, Song J, Forney CF, DeLong J, Rajcan I, Myles S (2016) QTL analysis of soft scald in two apple populations. Hortic Res 3:16043.  https://doi.org/10.1038/hortres.2016.43 CrossRefGoogle Scholar
  40. McClure KA, Gardner KM, Douglas GM, Song J, Forney CF, DeLong J, Fan L, Du L, Toivonen PMA, Somers DJ, Rajcan I, Myles S (2018) A genome-wide association study of apple quality and scab resistance. Plant Genome 11(1):170075.  https://doi.org/10.3835/plantgenome2017.08.0075 CrossRefGoogle Scholar
  41. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303 http://www.genome.org/cgi/doi/10.1101/gr.107524.110. Accessed 15 Jan 2013
  42. Migicovsky Z, Gardner KM, Money D, Sawler J, Bloom JS, Moffett P, Chao CT, Schwaninger H, Fazio G, Zhong GY, Myles S (2016) Genome to phenome mapping in apple using historical data. Plant Genome 9(2).  https://doi.org/10.3835/plantgenome2015.11.0113
  43. Moriya S, Iwanami H, Yamamoto T, Abe K (2011) A practical method for apple cultivar identification and parent-offspring analysis using simple sequence repeat markers. Euphytica 177:135–150.  https://doi.org/10.1007/s10681-010-0295-8 CrossRefGoogle Scholar
  44. Moriya S, Kunihisa M, Okada K, Iwanami H, Iwata H, Minamikawa M, Katayose Y, Matsumoto T, Mori S, Sasaki H, Matsumoto T, Nishitani C, Terakami S, Yamamoto T, Abe K (2017) Hortic J 86(2):159–170.  https://doi.org/10.2503/hortj.MI-156 CrossRefGoogle Scholar
  45. Mratinić E, Akšić MF (2012) Phenotypic diversity of apple (Malus sp.) germplasm in South Serbia. Braz Arch Biol Technol 55(3):349–358.  https://doi.org/10.1590/S1516-89132012000300004 CrossRefGoogle Scholar
  46. Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci 121(5):773–782CrossRefGoogle Scholar
  47. Nybom H, Schaal BA (1990) DNA “fingerprints” applied to paternity analysis in apples (Malus × domestica). Theor Appl Genet 79(6):763–768CrossRefGoogle Scholar
  48. Oraguzie NC, Gardiner SE, Basset HCM, Stefanati M, Ball RD, Bus VGM, White AG (2001) Genetic diversity and relationships in Malus sp. germplasm collections as determined by randomly amplified polymorphic DNA. J Am Soc Hortic Sci 126(3):318–328CrossRefGoogle Scholar
  49. Patzak J, Paprštein F, Henychová A, Sedlák J (2012) Comparison of genetic diversity structure analyses of SSR molecular marker data within apple (Malus × domestica) genetic resources. Genome 55:1–19.  https://doi.org/10.1139/g2012-054 CrossRefGoogle Scholar
  50. Pereira-Lorenzo S, Ramos-Cabrer AM, Ferreira V, Díaz-Hernández MB, Carnide V, Pinto-Carnide O, Rodrigues R, Velázquez-Barrera ME, Rios-Mesa D, Ascasíbar-Errasti J, Castro I (2018) Genetic diversity and core collection of Malus × domestica in northwestern Spain, Portugal and the Canary Islands by SSRs. Sci Hortic 240:49–56.  https://doi.org/10.1016/j.scienta.2018.05.053 CrossRefGoogle Scholar
  51. Pérez-Romero LF, Suárez MP, Dapena E, Rallo P (2015) Molecular and morphological characterization of local apple cultivars in Southern Spain. Genet Mol Res 14:1487–1501.  https://doi.org/10.4238/2015.February.20.4 CrossRefGoogle Scholar
  52. Potts SM, Han Y, Khan MA, Kushad MM, Rayburn AL, Korban SS (2012) Genetic diversity and characterization of a core collection of Malus germplasm using simple sequence repeats (SSRs). Plant Mol Biol Report 30:827–837.  https://doi.org/10.1007/s11105-011-0399-x CrossRefGoogle Scholar
  53. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909CrossRefGoogle Scholar
  54. Rehder A (1940) Manual of the cultivated trees and shrubs, 2nd edn. Revised and Enlarged, The Macmillan Company, New York, pp 389–399Google Scholar
  55. Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H (2013) SLAF-seq: an efficient method of large-scale De novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8(3):e58700.  https://doi.org/10.1371/journal.pone.0058700 CrossRefGoogle Scholar
  56. Sun R, Chang Y, Yang F, Wang Y, Li H, Zhao Y, Chen D, Wu T, Zhang X, Han Z (2015) A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality. BMC Genomics 16(747).  https://doi.org/10.1186/s12864-015-1946-x
  57. Urrestarazu J, Denancé C, Miranda C, Ravon E, Guyader A, Guisnel R (2016) Analysis of the genetic diversity and structure across a wide range of germplasm reveals prominent gene flow in apple at the European level. BMC Plant Biol 16:130.  https://doi.org/10.1186/s12870-016-0818-0 CrossRefGoogle Scholar
  58. Urrestarazu J, Muranty H, Denancé C, Leforestier D, Ravon E, Guyader A, Guisnel R, Feugey L, Aubourg S, Celton JM, Daccord N, Dondini L, Gregori R, Lateur M, Houben P, Ordidge M, Paprstein F, Sedlak J, Nybom H, Garkava-Gustavsson L, Troggio M, Bianco L, Velasco R, Poncet C, Théron A, Moriya S, Bink MCAM, Laurens F, Tartarini S, Durel CE (2017) Genome-wide association mapping of flowering and ripening periods in apple. Front Plant Sci 8(1923).  https://doi.org/10.3389/fpls.2017.01923
  59. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Ri AD, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42(10):833–841CrossRefGoogle Scholar
  60. Watillon B, Druart P, Du Jardin P, Kettmann R, Boxus P, Burny A (1991) Use of random cDNA probes to detect restriction fragment length polymorphisms among apple clones. Sci Hortic 46:235–243.  https://doi.org/10.1016/0304-4238(91)90046-2 CrossRefGoogle Scholar
  61. Zhang Q, Li J, Zhao Y, Korban SS, Han Y (2012) Evaluation of genetic diversity in Chinese wild apple species along with apple cultivars using SSR markers. Plant Mol Biol Report 30:539–546.  https://doi.org/10.1007/s11105-011-0366-6 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Yuansheng Chang
    • 1
  • Ping He
    • 1
  • Haibo Wang
    • 1
  • Huifeng Li
    • 1
  • Sen Wang
    • 1
  • Linguang Li
    • 1
    Email author
  1. 1.Shandong Institute of PomologyTai’anPeople’s Republic of China

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