Abstract
The apple genome sequence and the availability of high-throughput genotyping technologies have initiated a new era where SNP markers are abundant across the whole genome. Genomic selection (GS) is a statistical approach that utilizes all available genome-wide markers simultaneously to estimate breeding values or total genetic values. For breeding programmes, GS is a promising alternative to the traditional marker-assisted selection for manipulating complex polygenic traits often controlled by many small-effect genes. Various factors, such as genetic architecture of selection traits, population size and structure, genetic evaluation systems, density of SNP markers and extent of linkage disequilibrium, have been shown to be the key drivers of the accuracy of GS. In this paper, we provide an overview of the status of these aspects in current apple-breeding programmes. Strategies for GS for fruit quality and disease resistance are discussed, and an update on an empirical genomic selection study in a New Zealand apple-breeding programme is provided, along with a foresight of expected accuracy from such selection.
Similar content being viewed by others
References
Andersson L (2001) Genetic dissection of phenotypic diversity in farm animals. Nat Rev Genet 2:130–138
Beavis WD (1994) The power and deceit of QTL experiments: lessons from comparative QTL studies. Proceedings 49th Annual Corn and Sorghum Research Conference, Washington, pp 250–265
Bernardo R (2009) Genomewide selection for rapid introgression of exotic germplasm in maize. Crop Sci 49:419–425
Bink MCAM, Anderson AD, van de Weg WE, Thompson EA (2008) Comparison of marker-based pairwise relatedness estimators on a pedigreed plant population. Theor Appl Genet 117:843–855
Broggini GAL, Bus VGM, Parravicini G, Kumar S, Groenwold R, Gessler C (2010) Genetic mapping of 14 avirulence genes in an EU-B04 × 1639 progeny of Venturia inaequalis. Fungal Genet Bio 48:166–176
Browning SR, Browning BL (2010) High-Resolution detection of identity by descent in unrelated individuals. Am J Hum Genet 86:526–539
Bus VGM, Alspach PA, Hofstee ME, Brewer LR (2002a) Genetic variability and preliminary heritability estimates of resistance to scab (Venturia inaequalis) in an apple genetics population. NZ J Crop Hortic Sci 30:83–92
Bus VGM, Gardiner S, Weskett R, Ranatunga C, Samy A, Cook M, Rikkerink E (2002b) An update on apple scab resistance breeding in New Zealand. Acta Hortic 595:43–47
Bus VGM, Chagné D, Bassett HCM, Bowatte D, Calenge F, Celton JM, Durel C-E, Malone MT, Patocchi A, Ranatunga AC, Rikkerink EHA, Tustin DS, Zhou J, Gardiner SE (2008) Genome mapping of three major resistance genes to woolly aphid (Eriosoma lanigerum Hausm.). Tree Genet Genomes 4:223–236
Bus VGM, Esmenjaud D, Buck E, Laurens F (2009) Application of genetic markers in rosaceous crops. In: Folta KM, Gardiner SE (eds) Genetics and genomics of the rosaceae. Springer, New York, pp 563–600
Bus VGM, Bassett H, Bowatte D, Chagné D, Ranatunga C, Ulluwishewa D, Wiedow C, Gardiner S (2010) Genome mapping of an apple scab, a powdery mildew and a woolly apple aphid resistance gene from open-pollinated Mildew Immune Selection. Tree Genet Genomes 6:477–487
Calenge F, Durel CE (2006) Both stable and unstable QTLs for resistance to powdery mildew are detected in apple after four years of field assessments. Molec Breed 17:329–339
Calenge F, Faure A, Goerre M, Gebhardt C, van de Weg WE, Parisi L, Durel C-E (2004) Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379
Calenge F, Drouet D, Denancé C, van de Weg WE, Brisset MN, Paulin JP, Durel CE (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135
Calus M (2010) Genomic breeding value prediction: methods and procedures. Animal 4:157–164
Calus M, Veerkamp R (2007) Accuracy of breeding values when using and ignoring the polygenic effect in genomic breeding value estimation with a marker density of one SNP per cM. J Anim Breed Genet 124:362–368
Cardon LR, Bell JI (2001) Association study designs for complex diseases. Nat Rev Genet 2:91–99
Cevik V, King GJ (2002) High-resolution genetic analysis of the Sd-1 aphid resistance locus in Malus spp. Theor Appl Genet 105:346–354
Cevik V, Ryder CD, Popovich A, Manning K, King GJ, Seymour G (2009) A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.). Tree Genet Genomes 6:271–279
Chagné D, Carlisle C, Blond C, Volz RK, Whitworth CJ, Oraguzie NC, Crowhurst RN, Allan AC, Espley RV, Hellens RP, Gardiner SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212
Chagné D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EHA, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353–358
Conner JP, Brown SK, Weeden NF (1998) Molecular marker analysis of quantitative traits for growth and development in juvenile apple trees. Theor Appl Genet 96:1027–1035
Coster A, Bastiaansen JWM, Calus MPL, van Arendonk JAM, Bovenhuis H (2010) Sensitivity of methods for estimating breeding values using genetic markers to the number of QTL and distribution of QTL variance. Genet Sel Evol 42:9
Crossa J, de los Campos G, Pérez P, Gianola D, Burgueño J, Araus JL, Makumbi D, Singh RP, Dreisigacker S, Yan J, Arief V, Banziger M, Braun H-J (2010) Prediction of genetic values of quantitative traits in plant breeding using pedigree and molecular markers. Genetics 186:713–724
Davey MW, Kenis K, Keulemans J (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142:343–351
de los Campos G, Gianola D, Allison DB (2010) Predicting genetic predisposition in humans: the promise of whole-genome markers. Nature Rev Genet 11:880–886
Dekkers JCM (2004) Commercial application of marker- and gene-assisted selection in livestock: Strategies and lessons. J Anim Sci 82(E. Suppl):E313–E328
Dunemann F, Urbanietz A, Gardiner S, Bassett H, Legg W, Rusholme R, Bus V, Ranatunga C (2004) Marker assisted selection for Pl1 powdery mildew resistance in apple—Old markers for a new resistance gene. Acta Hortic 663:757–762
Dunemann F, Peil A, Urbanietz A, Garcia-Libreros T (2007) Mapping of the apple powdery mildew resistance gene Pl1 and its genetic association with an NBS-LRR candidate resistance gene. Plant Breed 126:476–481
Durel C-E, Laurens F, Fouillet A, Lespinasse Y (1998) Utilisation of pedigree information to estimate genetic parameters from large, unbalanced data sets in apple. Theor Appl Genet 96:1077–1085
Evans KM, James CM (2003) Identification of SCAR markers linked to Pl-w mildew resistance in apple. Theor Appl Genet 106:1178–1183
Fernando R, Grossman M (1989) Marker assisted selection using best linear unbiased prediction. Genet Select Evol 21:467–477
Flint J, Mackay TFC (2009) Genetic architecture of quantitative traits in flies, mice and humans. Genome Res 19:723–733
Gianola D, van Kaam J (2008) Reproducing kernel Hilbert spaces regression methods for genomic assisted prediction of quantitative traits. Genetics 178:2289–2303
Gianola D, de los Campos G, Hill WG, Manfredi E, Fernando R (2009) Additive genetic variability and the Bayesian alphabet. Genetics 183:347–363
Groen AF, Smith C (1995) A stochastic simulation study of the efficiency of marker-assisted introgression in livestock. J Anim Breed Genet 112:161–170
Habier D, Fernando RL, Dekkers JC (2007) The impact of genetic relationship information on genome-assisted breeding values. Genetics 177:2389–2397
Habier D, Tetens J, Seefried F-R, Lichtner P, Thaller G (2010) The impact of genetic relationship information on genomic breeding values in German Holstein cattle. Genet Sel Evol 42:5
Hampson CR, McNew R, Cline J, Embree C, Zandstra J, Wilson K (2009) Regional differences in performance of Canadian-bred apple cultivars and implications for breeding. Can J Plant Sci 89:81–91
Harada T, Sunako T, Wakasa Y, Soejima J, Satoh T, Niizeki M (2000) An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-ACS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theor Appl Genet 101:742–746
Harris BL, Johnson DL, Spelman RJ (2008) Genomic selection in New Zealand and the implications for national genetic evaluation. Proceedings 36th ICAR Session, Niagara Falls (USA), pp 325–331
Hayes BJ, Goddard ME (2001) The distribution of the effects of genes affecting quantitative traits in livestock. Genet Sel Evol 33:209–229
Hayes BJ, Bowman PJ, Chamberlain AJ, Goddard ME (2009) Invited review: Genomic selection in dairy cattle: Progress and challenges. J Dairy Sci 92:433–443
Hayes BJ, Pryce J, Chamberlain AJ, Bowman PJ, Goddard ME (2010a) Genetic architecture of complex traits and accuracy of genomic prediction: coat colour, milk-fat percentage, and type in Holstein cattle as contrasting model traits. PLoS Genet 6:e1001139
Hayes BJ, Daetwyler HD, Bowman P, Moser G, Tier B, Crump R, Khatkar M, Raadsma HW, Goddard ME (2010b) Accuracy of genomic selection: comparing theory and results. Proceedings of the Association for Advancement of Animal Breeding and Genetics, pp: 34–37
James CM, Clarke JB, Evans KM (2004) Identification of molecular markers linked to the mildew resistance gene Pl-d in apple. Theor Appl Genet 110:175–181
Jannink JL, Lorenz AJ, Iwata H (2010) Genomic selection in plant breeding: from theory to practice. Briefing Funct Genomics 9:166–177
Jung M, Ching A, Bhattramakki D, Dolan M, Tingey S, Morgante M, Rafalski A (2004) Linkage disequilibrium and sequence diversity in a 500-kbp region around the adh1 locus in elite maize germplasm. Theor Appl Genet 109:681–689
Kellerhals M, Dolega E, Koller B, Gessler C (2000) Advances in marker-assisted apple breeding. Acta Hortic 538:535–540
Kellerhals M, Kesper C, Koller B, Gessle C (2002) Breeding apples with durable disease resistance. In: Boos M (Ed.) Proceedings to the 10th International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture, 4–7 Feb. 2002, Weinsberg, Germany, pp 5–10
Kenis K, Keulemans J, Davey M (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661
Khan MA, Durel C-E, Duffy B, Drouet D, Kellerhals M, Gessler C, Patocchi A (2007) Development of molecular markers linked to the ‘Fiesta’ linkage group 7 major QTL for fire blight resistance and their application for marker-assisted selection. Genome 50:568–577
King GJ, Maliepaard C, Lynn JR, Alston FH, Durel C-E, Evans KM, Griffon B, Laurens F, Manganaris AG, Schrevens E, Tartarini S, Verhaegh J (2000) Quantitative genetic analysis and comparison of physical and sensory descriptors relating to fruit flesh firmness in apple (Malus pumila Mill.). Theor Appl Genet 100:1074–1084
King G, Lynn J, Dover CJ, Evans KM (2001) Resolution of quantitative trait loci for mechanical measures accounting for genetic variation in fruit texture of apple (Malus pumila Mill.). Theor Appl Genet 102:1227–1235
Kouassi AB, Durel C-E, Costa F, Tartarini S, van de Weg E, Evans K, Fernandez-Fernandez 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 Genomes 5:659–672
Kumar S (2006) Correlation between clonal means and open-pollinated seedling progeny means, and its implications for radiata pine breeding strategy. Can J For Res 36:1968–1975
Kumar S, Volz RK, Alspach PA, Bus VGM (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
Kumar S, Volz RK, Weskett R (2011) Genetic architecture of fruit quality traits in Malus x domestica (Borkh.) compared between own-rooted seedlings and vegetative propagules on ‘M. 9’ rootstock. Tree Genet Genomes doi:10.1007/s11295-011-0396-0
Lapins KO (1976) Inheritance of compact growth type in apple. J Am Soc Hort Sci 101:133–135
Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526
Lindgren D, Mullin TJ (1998) Relatedness and status number in seed orchard crops. Can J For Res 28:276–283
Luby JJ, Alspach PA, Bus VGM, Oraguzie NC (2002) Field resistance to fire blight in a diverse apple (Malus sp.) germplasm collection. J Am Soc Hortic Sci 127:245–253
Mackay TFC (2001) The genetic architecture of quantitative traits. Ann Rev Genet 35:303–339
Maliepaard C, Alston F, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73
Markussen T, Kruger J, Schmidt H, Dunemann F (1995) Identification of PCR-based markers linked to the powdery-mildew resistance gene Pl1 from Malus robusta in cultivated apple. Plant Breed 114:530–534
Meuwissen THE, Goddard ME (1996) The use of marker haplotypes in animal breeding schemes. Genet Sel Evol 28:161–176
Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
Micheletti D, Troggio M, Baldi P, Costa F, Pindo M, Komjanc M, Malnoy M, Zarkikh A, Magnago P, Velasco R, Salvi S (2010) LD estimation and analysis of diversity in apple. Proceeding of Plant and Animal Genomes XVIII Conference, San Diego, W255
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 Genomes doi:10.1007/s11295-011-0380-8
Moriya S, Iwanami H, Kotoda N, Takahashi S, Yamamoto T, Abe K (2009) Development of a marker-assisted selection system for columnar growth habit in apple breeding. J Jpn Soc Hort Sci 78:279–287
Moser G, Tier B, Crump R, Khatkar M, Raadsma H (2009) A comparison of five methods to predict genomic breeding values of dairy bulls from genome-wide SNP markers. Genet Sel Evol 41:56
Noiton DAM, Alspach PA (1996) Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J Am Soc Hortic Sci 121:773–782
Nybom N (1959) On the inheritance of acidity in cultivated apples. Heriditas 45:332–350
Ødegård J, Sonesson AK, Yazdi MH, Meuwissen THE (2009) Introgression of a major QTL from an inferior into a superior population using genomic selection. Genet Sel Evol 41:38
Oraguzie NC, Hofstee ME, Brewer LR, Howard C (2001) Estimation of genetic parameters in a recurrent selection programme in apple. Euphytica 118:29–37
Oraguzie NC, Iwanami H, Soejima J, Harada T, Hall A (2004) Inheritance of the Md-ACS1 gene and its relationship to fruit softening in apple (Malus × domestica Borkh.). Theor Appl Genet 108:1526–1533
Peil A, Garcia T, Richter K, Trognitz FC, Trognitz B, Hanke M-V, Flachowsky H (2007) Strong evidence for a fire blight resistance gene of Malus robusta located on linkage group 3 detected by rapid genome scanning. Plant Breed 126:470–475
Peil A, Hanke M-V, Flachowsky H, Richter K, Garcia-Libreros T, Celton J-M, Gardiner S, Horner M, Bus V (2008) Confirmation of the fire blight QTL of Malus x robusta 5 on linkage group 3. Acta Hortic 793:297–303
Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291
Plastow G, Sasaki S, Yu T-P, Deeb N, Prall G, Siggens K, Wilson E (2003) Practical application of DNA markers for genetic improvement, Proceedings of the 28th Annu. Mtg. Natl. Swine Improve. Fed. Iowa State University, Ames, pp 151–154
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Nat Acad Sci USA 98:11479–11484
Rothschild MF, Soller M (1997) Candidate gene analysis to detect genes controlling traits of economic importance in domestic livestock. Probe 8:13–20
Roux PMF, Khan MA, Broggini GAL, Duffy B, Gessler C, Patocchi A (2010) Mapping of quantitative trait loci for fire blight resistance in the apple cultivars ‘Florina’ and ‘Nova Easygro’. Genome 53:710–722
Rutkoski JE, Heffner EL, Sorrells ME (2011) Genomic selection for durable stem rust resistance in wheat. Euphytica 179:161–173
Segura V, Durel C-E, Costes E (2009) Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: QTL mapping. Tree Genet Genomes 5:165–179
Stoeckli S, Mody K, Gessler C, Patocchi A, Jermini M, Dorn S (2008) QTL analysis for aphid resistance and growth traits in apple. Tree Genet Genomes 4:833–847
Sved JA (1971) Linkage disequilibrium and homozygosity of chro mosome segments in finite populations. Theor Popul Biol 2:125–141
Thompson EA (2008) The IBD process along four chromosomes. Theor Popul Biol 73:369–373
VanRaden PM (2007) Efficient estimation of breeding values from dense genomic data. J Dairy Sci 90(suppl 1):374–375
VanRaden PM, Van Tassell CP, Wiggans GR, Sonstegard TS, Schnabel RD, Taylor JF, Schenkel FS (2009) Invited Review: Reliability of genomic predictions for North American Holstein bulls. J Dairy Sci 92:16–24
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genet 42:833–839
Volz RK, Rikkerink E, Austin P, Lawrence T, Bus VGM (2009) “Fast Breeding” in apple: a strategy to accelerate introgression of new traits into elite germplasm. Acta Hortic 814:163–168
Williams EB, Kuć J (1969) Resistance in Malus to Venturia inaequalis. Ann Rev Phytopathol 7:223–246
Xiang B, Li B (2003) Best linear unbiased prediction of clonal breeding values and genetic values from full-sib mating design. Can J For Res 33:2036–2043
Xu S (2003) Theoretical basis of the Beavis effect. Genetics 165:2259–2268
Xu SZ, Jia ZY (2007) Genomewide analysis of epistatic effects for quantitative traits in barley. Genetics 175:1955–1963
Yang JA, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR et al (2010) Common SNPs explain a large proportion of the heritability for human height. Nature Genet 42:565–U131
Zhu Y, Barritt BH (2008) Md-ACS1 and Md-ACO1 genotyping of apple (Malus x domestica Borkh.) \breeding parents and suitability for marker-assisted selection. Tree Genet Genomes 4:555–562
Acknowledgements
This work was partially funded by Prevar™ Limited under contract from the New Zealand Foundation for Research, Science and Technology. Luis Gea and Ron Beatson made many useful comments on an earlier version of this manuscript. D Chagné acknowledge support by USDA’s National Institute of Food and Agriculture—Speciality Crop Research Initiative RosBREED (2009-51181-05808) and European Framework Program 7 FruitBreedomics projects. The contribution of M. Bink was carried out as part of the EU COST Action TD0801 “StatSeq” and the FruitBreedomics project funded by the Commission of the European Communities (Contract FP7-KBBE-2010-265582). It does not necessarily reflect the Commission’s views and in no way anticipates its future policy in this area. Its content is the sole responsibility of the authors. We thank the anonymous reviewers and the Associate Editor for their suggestions on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Dirlewanger
Rights and permissions
About this article
Cite this article
Kumar, S., Bink, M.C.A.M., Volz, R.K. et al. Towards genomic selection in apple (Malus × domestica Borkh.) breeding programmes: Prospects, challenges and strategies. Tree Genetics & Genomes 8, 1–14 (2012). https://doi.org/10.1007/s11295-011-0425-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-011-0425-z