Tree Genetics & Genomes

, Volume 7, Issue 4, pp 857–868

Genetic diversity of the genus Malus and implications for linkage mapping with SNPs

  • Diego Micheletti
  • Michela Troggio
  • Andrey Zharkikh
  • Fabrizio Costa
  • Mickael Malnoy
  • Riccardo Velasco
  • Silvio Salvi
Original Paper

Abstract

Knowledge about the sequence-based genetic diversity of a crop species is important in order to develop highly informative genotyping assays, which will eventually positively impact breeding practice. Diversity data were obtained from two pools of 185 and 75 accessions each, representing most of the species belonging to the genus Malus, by re-sequencing 27 gene-specific amplicons and by screening 237 Malus × domestica SNPs using the multiplex genotyping technology SNPlex™. Nucleotide diversity and insertion/deletion rates in M. × domestica were estimated as π = 0.0037 and 1/333 bp, respectively. The SNP frequency was estimated as 0.0194 (1 SNP/52 bp) while within a single apple cultivar an average of one SNP in every 455 bp was found. We also investigated transferability (TSNP) of the heterozygous state of SNPs across the species M. × domestica and the genus Malus. Raw re-sequencing showed that 12–15% of M. × domestica SNPs are transferable to a second M. × domestica cultivar, however TSNP rose to ∼41% with SNPs selected for high minor allele frequency. TSNP of chosen SNPs averaged ∼27% in the two M. × domestica-related species, Malus sieversii and Malus sylvestris, but was much lower in more distantly related species. On the basis of TSNP, simulations, and empirical results, we calculated that a close-design, multiplexed genotyping array with at least 2,000 SNPs is required for building a highly saturated linkage maps within any M. × domestica cross. The same array would gradually lose informativeness in increasingly phylogenetically distant Malus species.

Keywords

Apple High-throughput genotyping SNP 

Supplementary material

11295_2011_380_MOESM1_ESM.pdf (113 kb)
Suppl. Table 1List of accessions (PDF 113 kb)
11295_2011_380_MOESM2_ESM.pdf (121 kb)
Suppl. Table 2Details on gene sequenced (PDF 121 kb)
11295_2011_380_MOESM3_ESM.pdf (145 kb)
Suppl. Table 3Details on TSNP (PDF 144 kb)

References

  1. Bérard A, Le Paslier MC, Dardevet M, Exbrayat-Vinson F, Bonnin I, Cenci A, Haudry A, Brunel D, Ravel C (2009) High-throughput single nucleotide polymorphism genotyping in wheat (Triticum spp.). Plant Biotechnol J 7:364–374PubMedCrossRefGoogle Scholar
  2. Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register JC 3rd, Tingey SV, Rafalski A (2002) Insertion-deletion polymorphisms in 3' regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547PubMedCrossRefGoogle Scholar
  3. Borevitz JO, Liang D, Plouffe D, Chang HS, Zhu T, Weigel D, Berry CC, Winzeler E, Chory J (2003) Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res 13:513–523PubMedCrossRefGoogle Scholar
  4. Brown SK (1992) Genetics of apple. Plant Breed Rev 9:333–366Google Scholar
  5. Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci USA 101:15255–15260PubMedCrossRefGoogle Scholar
  6. Chagné D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EH, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353–358PubMedCrossRefGoogle Scholar
  7. Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19PubMedCrossRefGoogle Scholar
  8. Deleu W, Esteras C, Roig C, González-To M, Fernández-Silva I, Gonzalez-Ibeas D, Blanca J, Aranda MA, Arús P, Nuez F, Monforte AJ, Picó MB, Garcia-Mas J (2009) A set of EST-SNPs for map saturation and cultivar identification in melon. BMC Plant Biol 9:90PubMedCrossRefGoogle Scholar
  9. Drost DR, Novaes E, Boaventura-Novaes C, Benedict CI, Brown RS, Yin T, Tuskan GA, Kirst M (2009) A microarray-based genotyping and genetic mapping approach for highly heterozygous outcrossing species enables localization of a large fraction of the unassembled Populus trichocarpa genome sequence. Plant J 58:1054–1067PubMedCrossRefGoogle Scholar
  10. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  11. Fan JB, Chee MS, Gunderson KL (2006) Highly parallel genomic assays. Nat Rev Genet 7:632–644PubMedCrossRefGoogle Scholar
  12. Feng TT, Zhou ZQ, Tang JM, Cheng MH, Zhou SL (2007) ITS sequence variation supports the hybrid origin of Malus toringoides Hughes. Can J Bot 85:659–666CrossRefGoogle Scholar
  13. Gilchrist EJ, Haughn GW, Ying CC, Otto SP, Zhuang J, Cheung D, Hamberger B, Aboutorabi F, Kalynyak T, Johnson L, Bohlmann J, Ellis BE, Douglas CJ, Cronk QC (2006) Use of Ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa. Mol Ecol 15:1367–1378PubMedCrossRefGoogle Scholar
  14. Glaszmann JC, Kilian B, Upadhyaya HD, Varshney RK (2010) Accessing genetic diversity for crop improvement. Curr Opin Plant Biol 13:167–173PubMedCrossRefGoogle Scholar
  15. Gu CC, Yu K, Ketkar S, Templeton AR, Rao DC (2008) On transferability of genome-wide tagSNP. Genet Epidemiol 32:89–97PubMedCrossRefGoogle Scholar
  16. Gupta PK, Rustgi S, Mir RR (2008) Array-based high-throughput DNA markers for crop improvement. Heredity 101:5–18PubMedCrossRefGoogle Scholar
  17. Han B, Xue Y (2003) Genome-wide intraspecific DNA-sequence variations in rice. Curr Opin Plant Biol 6:134–138PubMedCrossRefGoogle Scholar
  18. Hartl DL, Clark AG (2007) Principles of population genetics, Fourth editionth edn. Sinauer Associates, SunderlandGoogle Scholar
  19. Hosono S, Faruqi A, Dean FB, Du Y, Sun Z, Wu X, Du J, Kingsnore SF, Egholm M, Lasken R (2003) Unbiased whole-genome amplification directly from clinical samples. Genome Res 13:954–964PubMedCrossRefGoogle Scholar
  20. Hyten DL, Song Q, Choi IY, Yoon MS, Specht JE, Matukumalli LK, Nelson RL, Shoemaker RC, Young ND, Cregan PB (2008) High-throughput genotyping with the GoldenGate assay in the complex genome of soybean. Theor Appl Genet 116:945–952PubMedCrossRefGoogle Scholar
  21. Janick J, Cummins JV, Brown SK, Hemmat M (1996) Apples. In: Janick J, Moore JN (eds) Fruit breeding. Wiley, New York, pp 1–66Google Scholar
  22. Jiang D, Ye Q, Wang F, Cao L (2009) The mining of Citrus EST-SNP and its application in cultivar discrimination. Agric Sci China 9:179–190Google Scholar
  23. Jones E, Chu WC, Ayele M, Ho J, Bruggeman E, Yourstone K, Rafalksi A, Smith OS, McMullen MD, Bezawada C, Warren L, Babayev J, Basu S, Smith S (2009) Development of single nucleotide polymorphism (SNP) markers for use in commercial maize (Zea mais L.) germplasm. Mol Breed 24:165–176CrossRefGoogle Scholar
  24. Juniper BE, Mabberley DJ (2006) The story of the apple. Timber Press, Inc., PortlandGoogle Scholar
  25. Kolkman JM, Berry ST, Leon AJ, Slabaugh MB, Tang S, Gao W, Shintani DK, Burke JM, Knapp SJ (2007) Single nucleotide polymorphisms and linkage disequilibrium in sunflower. Genetics 177:457–468PubMedCrossRefGoogle Scholar
  26. Kota R, Varshney RK, Prasad M, Zhang H, Stein N, Graner A (2008) EST-derived single nucleotide polymorphism markers for assembling genetic and physical maps of the barley genome. Funct Integr Genomics 8:223–233PubMedCrossRefGoogle Scholar
  27. Laframboise T (2009) Single nucleotide polymorphism arrays: a decade of biological, computational and technological advances. Nucl Acids Res 37:4181–4193PubMedCrossRefGoogle Scholar
  28. Laurens F, Lespinasse Y, Fouillet A (2000) A new scab resistant apple: ‘Initial’. Acta Hort ISHS 538:707–710Google Scholar
  29. Lijavetzky D, Cabezas JA, Ibanez A, Rodriguez V, Martinez-Zapater JM (2007) High throughput SNP discovery and genotyping in grapevine (Vitis vinifera L.) by combining a re-sequencing approach and SNPlex technology. BMC Genomics 8:424PubMedCrossRefGoogle Scholar
  30. Lima L, Gramacho K, Carels N, Novais R, Gaiotto F, Lopes U, Gesteira A, Zaidan H, Cascardo J, Pires J, Micheli F (2009) Single nucleotide polymorphisms from Theobroma cacao expressed sequence tags associated with witches’ broom disease in cacao. Gen Mol Res 8:799–808CrossRefGoogle Scholar
  31. Lynch M, Walsh B (1997) Genetics and analysis of quantitative traits. Sinauer Associates, SunderlandGoogle Scholar
  32. Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci 121:773–782Google Scholar
  33. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217PubMedCrossRefGoogle Scholar
  34. Pindo M, Vezzulli S, Coppola G, Cartwright DA, Zharkikh A, Velasco R, Troggio M (2008) SNP high-throughput screening in grapevine using the SNPlex genotyping system. BMC Plant Biol 8:12PubMedCrossRefGoogle Scholar
  35. Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100PubMedCrossRefGoogle Scholar
  36. Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180PubMedCrossRefGoogle Scholar
  37. Robinson JP, Harris SA, Juniper BE (2001) Taxonomy of the genus Malus Mill. (Rosaceae) with emphasis on the cultivated apple, Malus domestica Borkh. Plant Syst Evol 226:35–58CrossRefGoogle Scholar
  38. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Meth Mol Biol 132:365–386Google Scholar
  39. Sachidanandam R, Weissman D, Schmidt SC, Kakol JM, Stein LD, Marth G, Sherry S, Mullikin JC, Mortimore BJ, Willey DL, Hunt SE, Cole CG, Coggill PC, Rice CM, Ning Z, Rogers J, Bentley DR, Kwok PY, Mardis ER, Yeh RT, Schultz B, Cook L, Davenport R, Dante M, Fulton L, Hillier L, Waterston RH, McPherson JD, Gilman B, Schaffner S, Van Etten WJ, Reich D, Higgins J, Daly MJ, Blumenstiel B, Baldwin J, Stange-Thomann N, Zody MC, Linton L, Lander ES, Altshuler D (2001) A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409:928–933PubMedCrossRefGoogle Scholar
  40. Staden R, Beal KF, Bonfield JK (2000) The Staden package, 1998. Meth Mol Biol 132:115–130Google Scholar
  41. Syvänen AC (2005) Toward genome-wide SNP genotyping. Nat Genet 37:S5–S10PubMedCrossRefGoogle Scholar
  42. Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166PubMedCrossRefGoogle Scholar
  43. Tobler A, Short S, Andersen M, Paner T, Briggs J, Lambert S, Wu P, Wang Y, Spoonde A, Koehler R, Peyret N, Chen C, Broomer A, Ridzon D, Zhou H, Hoo B, Hayashibara K, Leong L, Ma C, Rosenblum B, Day J, Ziegle J, De La Vega F, Rhodes M, Hennessy K, Wenz H (2005) The SNPlex genotyping system: a flexible and scalable platform for SNP genotyping. J Biomol Tech 16:398–406PubMedGoogle Scholar
  44. 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, Dal Ri A, 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 x domestica Borkh.). Nat Genet 42(10):833–839. doi: 10.1038/ng.654 Google Scholar
  45. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma TM, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Demattè L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando MS, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Peer Y, Salamini F, Viola R (2007) High quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326PubMedCrossRefGoogle Scholar
  46. Vezzulli S, Micheletti D, Riaz S, Pindo M, Viola R, This P, Walker MA, Troggio M, Velasco R (2008) A SNP transferability survey within the genus Vitis. BMC Plant Biol 8:128PubMedCrossRefGoogle Scholar
  47. Wu SB, Wirthensohn M, Hunt P, Gibson JP, Sedgley M (2008) High resolution melting analysis of almond SNPs derived from ESTs. Theor Appl Genet 118:1–14PubMedCrossRefGoogle Scholar
  48. Yamamoto T, Nagasaki H, Yonemaru J, Ebana K, Nakajima M, Shibaya T, Yano M (2010) Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms. BMC Genomics 11:267PubMedCrossRefGoogle Scholar
  49. Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4:e8451PubMedCrossRefGoogle Scholar
  50. Zhu Q, Zheng X, Luo J, Gaut BS, Ge S (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol Biol Evol 24:875–888PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Diego Micheletti
    • 1
  • Michela Troggio
    • 1
  • Andrey Zharkikh
    • 2
  • Fabrizio Costa
    • 1
  • Mickael Malnoy
    • 1
  • Riccardo Velasco
    • 1
  • Silvio Salvi
    • 1
    • 3
  1. 1.Istituto Agrario San Michele all’Adige, Research and Innovation Centre, Foundation Edmund MachTrentoItaly
  2. 2.Myriad GeneticsSalt Lake CityUSA
  3. 3.Department of Agroenvironmental Sciences and TechnologiesUniversity of BolognaBolognaItaly

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