Advertisement

Molecular Breeding

, Volume 34, Issue 2, pp 511–524 | Cite as

One-step reconstruction of multi-generation pedigree networks in apple (Malus × domestica Borkh.) and the parentage of Golden Delicious

  • Silvio Salvi
  • Diego Micheletti
  • Pierluigi Magnago
  • Marco Fontanari
  • Roberto Viola
  • Massimo Pindo
  • Riccardo VelascoEmail author
Article

Abstract

The increasing availability of genomic tools improves our ability to investigate the patterns of genetic diversity and relatedness among individuals. The pedigrees of many apple cultivars are completely unknown, often reducing the efficiency of breeding programs. Using a multilocus simple sequence repeat dataset, we applied a novel multi-generation pedigree-network reconstruction procedure based on the software FRANz in a Malus × domestica collection (101 cultivated and 22 wild apples) with partially known pedigree relationships. The procedure produced 78 parent–offspring relationships organized into three networks and showed high power for detecting real pedigree links (98.5 %) and a low false-positive rate (9.0 %). The largest reconstructed pedigree network spanned four generations and involved 65 cultivars. The availability of detailed pedigree connections confirmed that recent genealogical relationships affect population genetic structure in apple. Finally, our analysis enabled us to confirm or discard several pedigrees known only anecdotically, among which the cultivar Grimes Golden was validated as a parent of the widely grown cultivar Golden Delicious. The pedigree reconstruction protocol here described will be of broad applicability to other collections and crop species.

Keywords

Apple parentage Coancestry Pedigree reconstruction Population structure 

Notes

Acknowledgments

We thank Sue Gardiner for making available one additional source of Grimes Golden, and Enrico Ardizzoni for assistance in statistical analysis.

Supplementary material

11032_2014_54_MOESM1_ESM.doc (774 kb)
Supplementary material 1 (DOC 774 kb)

References

  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709PubMedCrossRefGoogle Scholar
  2. Almudevar A (2003) A simulated annealing algorithm for maximum likelihood pedigree reconstruction. Theor Pop Biol 63:63–75CrossRefGoogle Scholar
  3. Anderson EC, Garza JC (2006) The power of single nucleotide polymorphisms for large scale parentage inference. Genetics 172:2567–2582PubMedCentralPubMedCrossRefGoogle Scholar
  4. Baric S, Storti A, Hofer M, Dalla Via J (2012) Resolving the parentage of the apple cultivar ‘Meran’. Erwerbs-Obstbau 54:143–146CrossRefGoogle Scholar
  5. Bink M, Anderson A, van de Weg W, Thompson E (2008) Comparison of marker-based pairwise relatedness estimators on a pedigreed plant population. Theor Appl Genet 117:843–855PubMedCrossRefGoogle Scholar
  6. Bink MC, Totir LR, ter Braak CJ, Winkler CR, Boer MP, Smith OS (2012) QTL linkage analysis of connected populations using ancestral marker and pedigree information. Theor Appl Genet 124:1097–1113PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bowers JE, Meredith CP (1997) The parentage of a classic wine grape, Cabernet Sauvignon. Nat Genet 16:84–87PubMedCrossRefGoogle Scholar
  8. Brown SK (2012) Apple. In: Badenes ML, Byrne DH (eds) Fruit breeding—handbook of plant breeding, vol 8. Springer, Berlin, pp 329–360CrossRefGoogle Scholar
  9. Brown SK, Maloney KE (2003) Genetic improvement of apple: breeding, markers, mapping and biotechnology. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CAB International, Cambridge, pp 31–59Google Scholar
  10. Caballero A, Toro MA (2000) Interrelations between effective population size and other pedigree tools for the management of conserved populations. Genet Res 75:331–343PubMedCrossRefGoogle Scholar
  11. Cabe PR, Baumgaten A, Onan K, Luby JJ, Bedford DS (2005) Using microsatellite analysis to verify breeding records: a study of ‘Honeycrisp’ and other cold-hardy apple cultivars. HortScience 40:15–17Google Scholar
  12. Cervantes I, Pastor JM, Gutiérrez JP, Goyache F, Molina A (2011) Computing effective population size from molecular data: the case of three rare Spanish ruminant populations. Livest Sci 138:202–206CrossRefGoogle Scholar
  13. 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:e31745PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cipriani G, Spadotto A, Jurman I, Di Gaspero G, Crespan M, Meneghetti S, Frare E, Vignani R, Cresti M, Morgante M, Pezzotti M, Pe E, Policriti A, Testolin R (2010) The SSR-based molecular profile of 1005 grapevine (Vitis vinifera L.) accessions uncovers new synonymy and parentages, and reveals a large admixture amongst varieties of different geographic origin. Theor Appl Genet 121:1569–1585PubMedCrossRefGoogle Scholar
  15. Cornille A, Gladieux P, Smulders MJ, Roldán-Ruiz I, Laurens F, Le Cam B, Nersesyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang XG, Tenaillon MI, Giraud T (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):e1002703PubMedCentralPubMedCrossRefGoogle Scholar
  16. Cowell RG (2009) Efficient maximum likelihood pedigree reconstruction. Theor Pop Biol 76:285–291CrossRefGoogle Scholar
  17. Cowling WA (2013) Sustainable plant breeding. Plant Breed 132:1–9CrossRefGoogle Scholar
  18. Cussens J, Bartlett M, Jones EM, Sheehan NA (2013) Maximum likelihood pedigree reconstruction using integer linear programming. Genet Epidemiol 37:69–83PubMedCrossRefGoogle Scholar
  19. Durel CE, Laurens F, Fouillet A, Lespinasse Y (1998) Utilization of pedigree information to estimate genetic parameters from large unbalanced data sets in apple. Theor Appl Genet 96:1077–1085CrossRefGoogle 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 14:2611–2620PubMedCrossRefGoogle Scholar
  21. Evans KM, Patocchi A, Rezzonico F, Mathis F, Durel CE, Fenández-Fernández F, Boudichevskaia A, Dunemann F, Stankiewicz-Kosyl M, Gianfranceschi L, Komjanc M, Lateur M, Madduri M, Noor-dijk Y, van de Weg WE (2010) Genotyping of pedigreed apple breeding material with a genome-covering set of SSRs: trueness-to-type of cultivars and their parentages. Mol Breed 28:535–547CrossRefGoogle Scholar
  22. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Pearson Education Limited, Edinburgh GateGoogle Scholar
  23. Fischer C (2000) Multiple resistant apple cultivars and consequences for the apple breeding in the future. Acta Hort 538:229–234Google Scholar
  24. Gansner ER, Koutsofios E, North S (2009) Drawing graphs with dot. Technical report, AT&T Bell Laboratories, Murray HillGoogle Scholar
  25. Garkava-Gustavsson L, Kolodinska Brantestam A, Sehic J, Nybom H (2008) Molecular characterisation of indigenous Swedish apple cultivars based on SSR and S-allele analysis. Hereditas 145:99–112PubMedCrossRefGoogle Scholar
  26. Gharghani A, Zamani Z, Talaie A, Oraguzie NC, Fatahi R, Hajnajari H, Wiedow C, Gardiner SE (2009) Genetic identity and relationships of Iranian apples (Malus × domestica Borkh) cultivars and landraces, wild apple species and representative old apple cultivars based on SSR markers. Genet Resour Crop Evol 56:829–842CrossRefGoogle Scholar
  27. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
  28. Hampson CR, Kemp H (2003) Characteristics of important commercial apple cultivars. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CAB International, CambridgeGoogle Scholar
  29. Iwanami H, Moriya S, Kotoda N, Mimida N, Sumiyoshi ST, Abe K (2012) Mode of inheritance in fruit acidity in apple analysed with a mixed model of a major gene and polygenes using large complex pedigree. Plant Breed 131:322–328CrossRefGoogle Scholar
  30. Jones OR, Wang J (2010) Molecular marker-based pedigrees for animal conservation biologists. Anim Conserv 13:26–34CrossRefGoogle Scholar
  31. Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Resour 10:6–30PubMedCrossRefGoogle Scholar
  32. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  33. Khanizadeh S, Cousineau J (1998) Our apples. Agriculture and Agri-Food Canada, St-Jean-sur-RichelieuGoogle Scholar
  34. Kitahara K, Matsumoto S, Yamamoto T, Soejima J, Komára T, Komatu H, Abe K (2005) Parent identification of eight apple cultivars by S-RNase analysis and simple sequence repeat markers. HortScience 40:314–317Google Scholar
  35. Kodama M, Hard JJ, Naish KA (2012) Temporal variation in selection on body length and date of return in a wild population of coho salmon, Oncorhynchus kisutch. BMC Evol Biol 12:116PubMedCentralPubMedCrossRefGoogle Scholar
  36. Kouassi AB, Durel CE, Costa F, Tartarini S, van de Weg E, Evans K, Fernández-Fernández F, Govan C, Boudichevskaja A, Dunemann F, Antofie A, Lateur M, Stankiewicz-Kosyl M, Soska A, Tomala K, Lewandowski M, Rutkovski K, Zurawicz E, Guerra W, Laurens F (2009) Estimation of genetic parameters and prediction of breeding values for apple fruit-quality traits using pedigreed plant material in Europe. Tree Genet Genomics 5:659–672CrossRefGoogle Scholar
  37. Kumar S, Garrick DJ, Bink MC, Whitworth C, Chagné D, Volz RK (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genom 14:393CrossRefGoogle Scholar
  38. Lacombe T, Boursiquot JM, Laucou V, Di Vecchi-Staraz M, Péros JP, This P (2013) Large-scale parentage analysis in an extended set of grapevine cultivars (Vitis vinifera L.). Theor Appl Genet 126:401–414PubMedCrossRefGoogle Scholar
  39. Lacy RC (1995) Clarification of genetic terms and their use in the management of captive populations. Zoo Biol 14:565–577CrossRefGoogle Scholar
  40. Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10:217–241CrossRefGoogle Scholar
  41. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129PubMedCrossRefGoogle Scholar
  42. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedCentralPubMedGoogle Scholar
  43. Micheletti D, Troggio M, Zharkikh A, Costa F, Malnoy M, Velasco R, Salvi S (2011) Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genet Genom 7:857–868CrossRefGoogle Scholar
  44. Miyamoto MM, Allen JM, Gogarten JF, Chapman CA (2013) Microsatellite DNA suggests that group size affects sex-biased dispersal patterns in Red Colobus monkeys. Am J Primatol 75:478–490PubMedCentralPubMedCrossRefGoogle Scholar
  45. Moriya S, Iwanami H, Okada K, Yamamoto T, Abe K (2011) A practical method for apple cultivar identification and parent-offspring analysis using simple sequence repeat markers. Euphytica 177:135–150CrossRefGoogle Scholar
  46. Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hort Sci 121:773–782Google Scholar
  47. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  48. Percival DC, Proctor JTA (1994) ‘Golden Delicious’ progeny: 21st century apples. Fruit Var J 48:58–62Google Scholar
  49. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes consequences, and solutions. Nat Rev Genet 6:847–859PubMedCrossRefGoogle Scholar
  50. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  51. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  52. Rafalski JA (2011) Genomic tools for the analysis of genetic diversity. Plant Genet Res 9:159–162CrossRefGoogle Scholar
  53. Riester M, Stadler PF, Klemm K (2009) FRANz: reconstruction of wild multi-generation pedigrees. Bioinformatics 25:2134–2139PubMedCentralPubMedCrossRefGoogle Scholar
  54. Sawamura Y, Takada N, Yamamoto T, Saito T, Kimura T, Kotobuki K (2008) Identification of parent-offspring relationships in 55 Japanese pear cultivars using S-Rnase allele and SSR markers. J Jpn Soc Hort Sci 77:364–373CrossRefGoogle Scholar
  55. Sitther V, Zhang D, Dhekney SA, Harris DL, Yadav AK, Okie WR (2012) Cultivar identification, pedigree verification, and diversity analysis among peach cultivars based on simple sequence repeat markers. J Am Soc Hort Sci 137:114–121CrossRefGoogle Scholar
  56. Smith MWG (1971) The national apple register of the United Kingdom. Ministry of Agriculture, Fisheries, and Food, LondonGoogle Scholar
  57. Thomas SC (2005) The estimation of genetic relationships using molecular markers and their efficiency in estimating heritability in natural populations. Phil Trans R Soc B 360:1457–1467PubMedCentralPubMedCrossRefGoogle Scholar
  58. Townsend SM, Jamieson IG (2013) Molecular and pedigree measures of relatedness provide similar estimates of inbreeding depression in a bottlenecked population. J Evol Biol 26:889–899PubMedCrossRefGoogle Scholar
  59. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935PubMedCrossRefGoogle Scholar
  60. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839PubMedCrossRefGoogle Scholar
  61. Wang J, Santure A (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1–16CrossRefGoogle Scholar
  62. Weir BS (1996) Genetic data analysis II. Sinauer Associates, SunderlandGoogle Scholar
  63. Weir BS, Anderson AD, Hepler AB (2006) Genetic relatedness analysis: modern data and new challenges. Nat Rev Genet 7:771–780PubMedCrossRefGoogle Scholar
  64. Wright S (1922) Coefficients of inbreeding and relationship. Am Nat 56:330–338CrossRefGoogle Scholar
  65. Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Silvio Salvi
    • 1
    • 2
  • Diego Micheletti
    • 1
  • Pierluigi Magnago
    • 1
  • Marco Fontanari
    • 1
  • Roberto Viola
    • 1
  • Massimo Pindo
    • 1
  • Riccardo Velasco
    • 1
    Email author
  1. 1.Centre for Research and InnovationFondazione Edmund MachSan Michele all’AdigeItaly
  2. 2.Department of Agricultural ScienceUniversity of BolognaBolognaItaly

Personalised recommendations