Skip to main content
Log in

Epistatic fire blight resistance QTL alleles in the apple cultivar ‘Enterprise’ and selection X-6398 discovered and characterized through pedigree-informed analysis

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Most cultivated apple cultivars are highly susceptible to fire blight, caused by Erwinia amylovora. However, differences in resistance levels are observed among cultivars and could be used in breeding. In this paper, we investigated the genetic basis of fire blight resistance of the cultivar ‘Enterprise’ and the advanced breeding selection X-6398. Genotyped pedigrees were used for validating and curating historic pedigree records. Various quantitative trait locus (QTL) discovery approaches were applied on the full-sib families ‘Gala’ × ‘Enterprise’ (GaEn) and X-6398 × X-6683 (IW) with the software FlexQTL™ and MapQTL®. The paternal lineage of ‘Enterprise’ was reconstructed and showed to include ‘Cox’s Orange Pippin’. The QTLs found varied with the software used. Using FlexQTL™, two were found on linkage groups (LGs) 7 and 13, favourable alleles inherited by Enterprise from ‘Cox’s Orange Pippin’ and ‘Golden Delicious’, respectively. The former was identical to the previously named FB_F7 allele from ‘Fiesta’, while the latter is new and has been named FB_13GD. X-6398 had a QTL at the same position as FB_F7. Its favourable allele was new, originating from the unknown grandfather of X-4598, and was named FB_7X-6398. Using MapQTL® on GaEn, FB_F7 was also identified. Performing the same analysis on the subset of offspring that carried the favourable allele of FB_F7, two putative QTLs on LG8 and on top of LG13 were identified, which showed interactions with FB_F7. Implication of the findings for breeding for fire blight-resistant apples is discussed. Single nucleotide polymorphism data on Enterprise and its ancestors are provided.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmadi N, Albar L, Pinel PG, Fargette D, Ghesquière A (2001) Genetic basis and mapping of the resistance to rice yellow mottle virus. III. Analysis of QTL efficiency in introgressed progenies confirmed the hypothesis of complementary epistasis between two resistance QTLs. Theor Appl Genet 103:1084–1092

    Article  CAS  Google Scholar 

  • Allard A, Bink MCAM, Martinez S, Kelner JJ, Legave JM, Di Guardo M et al (2016) Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. J Exp Bot 67(9):2875–2888. https://doi.org/10.1093/jxb/erw130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baumgartner IO, Patocchi A, Frey JE, Peil A, Kellerhals M (2015a) Breeding elite lines of apple carrying pyramided homozygous resistance genes against apple scab and resistance against powdery mildew and fire blight. Plant Mol Biol Rep 33(5):1573–1583. https://doi.org/10.1007/s11105-015-0858-x

    Article  CAS  Google Scholar 

  • Baumgartner IO, Patocchi A, Lussi L, Kellerhals M, Peil A (2015b) Accelerated introgression of fire blight resistance from Malus × robusta 5 and other wild germplasm into elite apples. Acta Hortic 1056:281–287

    Google Scholar 

  • Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotech 32:76–84. https://doi.org/10.1016/j.copbio.2014.11.007

    Article  CAS  PubMed  Google Scholar 

  • 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 CE, Troggio M (2016) Development and validation of the Axiom® Apple 480K SNP genotyping array. Plant J 86(1):62–74. https://doi.org/10.1111/tpj.13145

    Article  CAS  PubMed  Google Scholar 

  • Bianco L, Cestaro A, Sargent DJ, Banchi E, Derdak S, Di Guardo M, Salvi S, Jansen J, Viola R, Gut I, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bink MCAM, Boer MP, ter Braak CJF, Jansen J, Voorrips RE, van de Weg E (2008) Bayesian analysis of complex traits in pedigreed plant populations. Euphytica 161(1-2):85–96. https://doi.org/10.1007/s10681-007-9516-1

    Article  Google Scholar 

  • Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel CE, Kouassi AB et al (2014) Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet 127(5):1073–1090. https://doi.org/10.1007/s00122-014-2281-3

    CAS  PubMed  Google Scholar 

  • Bink MCAM, van Eeuwijk FA (2009) A Bayesian QTL linkage analysis of the common dataset from the 12th QTLMAS workshop. BMC Proc 3:4

    Article  Google Scholar 

  • Bourguet D, Delmotte F, Franck P, Guillemaud T, Reboud X, Vacher C, et al. (2016) Combining selective pressures to enhance the durability of disease resistance genes. Frontiers in Plant Science 7

  • Broggini GAL, Wöhner T, Fahrentrapp J, Kost TD, Flachowsky H, Peil A, Hanke MV, Richter K, Patocchi A, Gessler C (2014) Engineering fire blight resistance into the apple cultivar 'Gala' using the FB_MR5 CC-NBS-LRR resistance gene of Malus x robusta 5. Plant Biotechnol J 12(6):728–733. https://doi.org/10.1111/pbi.12177

    Article  CAS  PubMed  Google Scholar 

  • Brun H, Chevre AM, Fitt BDL, Powers S, Besnard AL, Ermel M et al (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185(1):285–299. https://doi.org/10.1111/j.1469-8137.2009.03049.x

    Article  PubMed  Google Scholar 

  • Bühlmann A, Gassmann J, Ingenfeld A, Hunziker K, Kellerhals M, Frey JE (2015) Molecular characterisation of the Swiss fruit genetic resources. Erwerbs-obstbau 57(1):29–34. https://doi.org/10.1007/s10341-015-0230-1

    Article  Google Scholar 

  • Caffier V, Lasserre-Zuber P, Giraud M, Lascostes M, Sievenard R, Le Marquand A et al (2014) Erosion of quantitative host resistance in the apple x Venturia inaequalis pathosystem. Infect Genet Evol 27:481–489. https://doi.org/10.1016/j.meegid.2014.02.003

    Article  PubMed  Google Scholar 

  • Calenge F, Drouet D, Denance C, van de Weg WE, Brisset M-N, Paulin J-P et al (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. Gene 111:128–135

    CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Chagné D, Kirk C, Whitworth C, ErasmusonRoss S, Bicknell R, Sargent DJ et al (2015) Polyploid and aneuploid detection in apple using a single nucleotide polymorphism array. Tree Genet Genomes 11(5):94. https://doi.org/10.1007/s11295-015-0920-8

    Article  Google Scholar 

  • Crosby JA, Janick J, Pecknold PC (1994) ‘GoldRush’ apple. Hotscience 29:827–828

    Google Scholar 

  • de Koning D-J, McIntyre LM (2017) Back to the future: multiparent populations provide the key to unlocking the genetic basis of complex traits. G3: Genes Genom Genet 7:1617–1618

    Google Scholar 

  • Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R, di Pierro EA, Gouzy J, Rees DJG, Guérif P, Muranty H, Durel CE, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, van de Weg E, Troggio M, Bucher E (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49(7):1099–1106. https://doi.org/10.1038/ng.3886

    Article  CAS  PubMed  Google Scholar 

  • Di Guardo M, Bink M, Guerra W, Letschka T, Lozano L, Busatto N et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  • Di Guardo M, Micheletti D, Bianco L, Koehorst-van Putten HJJ, Longhi S, Costa F et al (2015) ASSIsT: an automatic SNP scoring tool for in- and outbreeding species. Bioinformatics 31(23):3873–3874. https://doi.org/10.1093/bioinformatics/btv446

    PubMed  PubMed Central  Google Scholar 

  • Di Pierro EA, Gianfranceschi L, Di Guardo M, Koehorst-van Putten HJJ, Kruisselbrink JW, Longhi S et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  • Durand JB, Allard A, Guitton B, van de Weg E, Bink MCAM, Costes E (2017) Predicting flowering behavior and exploring its genetic determinism in an apple multi-family population based on statistical indices and simplified phenotyping. Frontiers 8:858. https://doi.org/10.3389/fpls.2017.00858

    Google Scholar 

  • Durel CE, Denancé C, Brisset MN (2009) Two distinct major QTL for resistance to fire blight co-localize on linkage group 12 in apple genotypes ‘Evereste’ and Malus floribunda clone 821. Genome 52(2):139–147. https://doi.org/10.1139/G08-111

    Article  CAS  PubMed  Google Scholar 

  • Emeriewen O, Richter K, Kilian A, Zini E, Hanke MV, Malnoy M, Peil A (2014) Identification of a major quantitative trait locus for resistance to fire blight in the wild apple species Malus fusca. Mol Breed 34(2):407–419. https://doi.org/10.1007/s11032-014-0043-1

    Article  CAS  Google Scholar 

  • Evans KM, Patocchi A, Rezzonico F, Mathis F, Durel CE, Fernandez-Fernandez F et al (2011) Genotyping of pedigreed apple breeding material with a genome-covering set of SSRs: trueness-to-type of cultivars and their parentages. Mol Breed 28(4):535–547. https://doi.org/10.1007/s11032-010-9502-5

    Article  Google Scholar 

  • Fahrentrapp J, Broggini GAL, Kellerhals M, Peil A, Richter K, Zini E, Gessler C (2013) A candidate gene for fire blight resistance in Malus x robusta 5 is coding for a CC-NBS-LRR. Tree Genet Genomes 9(1):237–251. https://doi.org/10.1007/s11295-012-0550-3

    Article  Google Scholar 

  • Fazio G, Aldwinckle H, Volk G, Richards C, Janisiewicz W, Forsline P (2009) Progress in evaluating Malus sieversii for disease resistance and horticultural traits. Acta Hortic 814:59–66

    Article  Google Scholar 

  • Flachowsky H, Hanke MV, Peil A, Strauss SH, Fladung M (2009) A review on transgenic approaches to accelerate breeding of woody plants. Plant Breed 128(3):217–226. https://doi.org/10.1111/j.1439-0523.2008.01591.x

    Article  CAS  Google Scholar 

  • Flachowsky H, Le Roux P-M, Peil A, Patocchi A, Richter K, Hanke M-V (2011) Application of a high-speed breeding technology to apple (Malus × domestica) based on transgenic early flowering plants and marker-assisted selection. New Phytol 192(2):364–377. https://doi.org/10.1111/j.1469-8137.2011.03813.x

    Article  CAS  PubMed  Google Scholar 

  • Fresnedo-Ramírez J, Bink MCAM, van de Weg E, Famula TR, Crisosto CH, Frett TJ et al (2015) QTL mapping of pomological traits in peach and related species breeding germplasm. Mol Breed 35:1–19

    Article  Google Scholar 

  • Fresnedo-Ramírez J, Frett TJ, Sandefur PJ, Salgado-Rojas A, Clark JR, Gasic K, Peace CP, Anderson N, Hartmann TP, Byrne DH, Bink MCAM, van de Weg E, Crisosto CH, Gradziel TM (2016) QTL mapping and breeding value estimation through pedigree-based analysis of fruit size and weight in four diverse peach breeding programs. Tree Genet Genomes 12(2):25. https://doi.org/10.1007/s11295-016-0985-z

    Article  Google Scholar 

  • Guan Y, Peace C, Rudell D, Verma S, Evans K (2015) QTLs detected for individual sugars and soluble solids content in apple. Mol Breeding 35(6):135. https://doi.org/10.1007/s11032-015-0334-1

    Article  Google Scholar 

  • Hernández Mora JR, Micheletti D, Bink M, Van de Weg E, Bassi D, Nazzicari N et al (2017) Integrated QTL detection for key breeding traits in multiple peach progenies. BMC Genomics 18(1):404. https://doi.org/10.1186/s12864-017-3783-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard N, van de Weg E, Bedford D, Peace C, Vanderzande S, Clark M et al (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 dataset. Hortic Res 4:17003. https://doi.org/10.1038/hortres.2017.3

    Article  PubMed  PubMed Central  Google Scholar 

  • Islam MA, Alam J, Urmee SA, Rahaman MH, Razu MH, Mazumdar RM (2014) Isolation, identification, in-vitro antibiotic resistance and plant extract sensitivity of fire blight causing Erwinia amylovora. J Plant Pathol Microb 5:3

    Google Scholar 

  • Janick J (2006) The PRI apple breeding program. Hortscience 41:8–10

    Google Scholar 

  • Jänsch M, Frey JE, Hilber-Bodmer M, Broggini GAL, Weger J, Schnabel G, Patocchi A (2012) SSR marker analysis of Monilinia fructicola from Swiss apricots suggests introduction of the pathogen from neighboring countries and the United States. Plant Pathol 61(2):247–254. https://doi.org/10.1111/j.1365-3059.2011.02511.x

    Article  Google Scholar 

  • Kellerhals M, Szalatnay D, Hunziker K, Duffy B, Nybom H, Ahmadi-Afzadi M, Höfer M, Richter K, Lateur M (2012) European pome fruit genetic resources evaluated for disease resistance. Trees 26(1):179–189. https://doi.org/10.1007/s00468-011-0660-9

    Article  Google Scholar 

  • Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breed 17(4):299–306. https://doi.org/10.1007/s11032-006-9000-y

    Article  Google Scholar 

  • Khan MA, Durel CE, 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(6):568–577. https://doi.org/10.1139/G07-033

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Han Y, Zhao YF, Korban SS (2012) A high-throughput apple SNP genotyping platform using the GoldenGate™ assay. Gene 494(2):196–201. https://doi.org/10.1016/j.gene.2011.12.001

    Article  CAS  PubMed  Google Scholar 

  • Korban SS, Ries SM, Klopmeyer MJ, Morrisey JF, Hattermann DR (1988) Genotypic responses of scab-resistant apple cultivars/selections to two strains of Erwinia amylovora and the inheritance of resistance to fire blight. Ann Appl Biol 113(1):101–105. https://doi.org/10.1111/j.1744-7348.1988.tb03286.x

    Article  Google Scholar 

  • Kost TD, Gessler C, Jänsch M, Flachowsky H, Patocchi A, Broggini GAL (2015) Development of the first cisgenic apple with increased resistance to fire blight. PLoS One 10:12

    Article  Google Scholar 

  • Larsen B, Toldam-Andersen BT, Pedersen C, Ørgaard M (2017) Unravelling genetic diversity and cultivar parentage in the Danish apple gene bank collection. Tree Genet Genom 13(1):14. https://doi.org/10.1007/s11295-016-1087-7

    Article  Google Scholar 

  • 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 Rep 34(4):827–844. https://doi.org/10.1007/s11105-015-0966-7

    Article  CAS  Google Scholar 

  • Laurens F, Durel C-E, Patocchi A, Peil A, Salvi S, Tartarini S et al (2010) Review on apple genetics and breeding programmes and presentation of a new European initiative to increase fruit breeding efficiency. J Fruit Sci 27:102–107

    Google Scholar 

  • Le Roux PM, 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(9):710–722. https://doi.org/10.1139/G10-047

    Article  PubMed  Google Scholar 

  • Leumann L, Baumgartner I, Lussi L, Frey L, Nölly M, Kellerhals M (2013) Ladina, die neue feuerbrandrobuste Apfelsorte. Schweiz Z Obst-Weinbau 1:10–13

    Google Scholar 

  • Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E et al (2002) Development and characterization of 140 new microsatellites in apple (Malus x domestica Borkh.) Mol Breed 10(4):217–241. https://doi.org/10.1023/A:1020525906332

    Article  CAS  Google Scholar 

  • Mangandi J, Verma S, Osorio L, Peres NA, van de Weg E, Whitaker V (2017) Pedigree-based analysis in a multiparental population of octoploid strawberry reveals QTL alleles conferring resistance to Phytophthora cactorum. G3: Genes Genom Genet 7:1707–1719

    Google Scholar 

  • McGhee GC, Sundin GW (2011) Evaluation of Kasugamycin for fire blight management, effect on nontarget bacteria, and assessment of Kasugamycin resistance potential in Erwinia amylovora. Phytophatol 101(2):192–204. https://doi.org/10.1094/PHYTO-04-10-0128

    Article  CAS  Google Scholar 

  • McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40(1):443–465. https://doi.org/10.1146/annurev.phyto.40.120301.093927

    Article  CAS  PubMed  Google Scholar 

  • Milčevičová R, Gosch C, Halbwirth H, Stich K, Hanke MV, Peil A, Flachowsky H, Rozhon W, Jonak C, Oufir M, Hausman JF, Matušíková I, Fluch S, Wilhelm E (2010) Erwinia amylovora-induced defense mechanisms of two apple species that differ in susceptibility to fire blight. Plant Sci 179(1-2):60–67. https://doi.org/10.1016/j.plantsci.2010.04.013

    Article  Google Scholar 

  • Nybom H, Mikicin A, Garkava-Gustavsson L, Sehic J, Lewandowski M, Sobiczewski P (2011) Assessment of fire blight tolerance in apple based on plant inoculations with Erwinia amylovora and DNA markers. Trees 26:199–213

    Article  Google Scholar 

  • Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 183(1):190–199. https://doi.org/10.1111/j.1469-8137.2009.02827.x

    Article  CAS  PubMed  Google Scholar 

  • Parravicini G, Gessler C, Denance C, Lasserre-Zuber P, Vergne E, Brisset MN et al (2011) Identification of serine/threonine kinase and nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes in the fire blight resistance quantitative trait locus of apple cultivar 'Evereste. Mol Plant Pathol 12(5):493–505. https://doi.org/10.1111/j.1364-3703.2010.00690.x

    Article  CAS  PubMed  Google Scholar 

  • Paulin JP, Samson R (1973) Le feu bactérien en France. II. Caractères des souches d’Erwinia amylovora (Burrill), Winslow et al. 1920, isolées du foyer Franco-Belge. Ann Phytopathol 5:389–397

    Google Scholar 

  • Peace C, Luby J, van de Weg EW, Bink MCAM, Iezzoni A (2014) A strategy for developing representative germplasm sets for systematic QTL validation, demonstrated for apple, peach, and sweet cherry. Tree Genet Genomes: DOI https://doi.org/10.1007/s11295-014-0788-z

  • Peil A, Garcia-Libreros T, Richter K, Trognitz FC, Trognitz B, Hanke MV, Flachowsky H (2007) Strong evidence for a fire blight resistance gene of Malus robusta located on linkage group 3. Plant Breed 126(5):470–475. https://doi.org/10.1111/j.1439-0523.2007.01408.x

    Article  CAS  Google Scholar 

  • Peil A, Wöhner T, Hanke MV, Flachowsky H, Richter K, Wensing A, Emeriewen O, Malnoy M, LeRoux PM, Patocchi A (2013) Comparative mapping of fire blight resistance in Malus. Acta Hortic 1056:47–51

    Google Scholar 

  • Perchepied L, Guérif P, Ravon E, Denancé C, Laurens F, Robert P et al (2016) Polygenic inheritance of resistance to Cacopsylla pyri in a Pyrus communis × P. ussuriensis progeny is explained by three QTLs involving an epistatic interaction. Tree Genet Genom 12:108

    Article  Google Scholar 

  • Pikunova A, Madduri M, Sedov E, Noordijk Y, Peil A, Troggio M, Bus VGM, G.F. Visser R, van de Weg E (2014) Schmidt’s Antonovka’ is identical to ‘Common Antonovka’, an apple cultivar widely used in Russia in breeding for biotic and abiotic stresses. Tree Genet Genomes 10(2):261–271. https://doi.org/10.1007/s11295-013-0679-8

    Article  Google Scholar 

  • Quenouille J, Paulhiac E, Moury B, Palloix A (2014) Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants. Heredity 112(6):579–587. https://doi.org/10.1038/hdy.2013.138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richter K, Fischer C (2002) Stability of fire blight resistance in apple. Acta Hortic 590:381–384

    Article  Google Scholar 

  • Roach JA, Verma S, Peres NA, Jamieson AR, van de Weg WE, Bink MCAM, Bassil NV, Lee S, Whitaker VM (2016) FaRXf1: a locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry. Theor Appl Genet 129(6):1191–1201. https://doi.org/10.1007/s00122-016-2695-1

    Article  CAS  PubMed  Google Scholar 

  • Rosyara UR, Bink MCAM, van de Weg E, Guorong Z, Dechun W, Audrey S et al (2013) Fruit size QTL identification and the prediction of parental QTL genotypes and breeding values in multiple pedigreed populations of sweet cherry. Mol Breed 32(4):875–877. https://doi.org/10.1007/s11032-013-9916-y

    Article  Google Scholar 

  • Salvi S, Micheletti D, Magnago P, Fontanari M, Viola R, Pindo M, Velasco R (2014) One-step reconstruction of multi-generation pedigree networks in apple (Malus x domestica Borkh.) and the parentage of Golden Delicious. Mol Breed 34(2):511–524. https://doi.org/10.1007/s11032-014-0054-y

    Article  CAS  Google Scholar 

  • Schouten H, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7(8):750–753. https://doi.org/10.1038/sj.embor.7400769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet Genomes 2(4):202–224. https://doi.org/10.1007/s11295-006-0045-1

    Article  Google Scholar 

  • Urrestarazu J, Denancé C, Ravon E, Guyader A, Guisnel R, Feugey L, Poncet C, Lateur M, Houben P, Ordidge M, Fernandez-Fernandez F, Evans KM, Paprstein F, Sedlak J, Nybom H, Garkava-Gustavsson L, Miranda C, Gassmann J, Kellerhals M, Suprun I, Pikunova AV, Krasova NG, Torutaeva E, Dondini L, Tartarini S, Laurens F, Durel CE (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(1):130. https://doi.org/10.1186/s12870-016-0818-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanneste JL, ed. (2000) Fire blight: the disease and its causative agent, Erwinia amylovora. Wallingford, UK: CABI Publ

  • Van Ooijen JW, Kyazma BV. MapQTL® 6 (2009) Software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV: Wageningen, Netherlands

  • 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. https://doi.org/10.1038/ng.654

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE, Bink MCAM, Kruisselbrink JW, Koehorst-van Putten HJ, van de Weg WE (2016) PediHaplotyper: software for consistent assignment of marker haplotypes in pedigrees. Mol Breed 36(8):119. https://doi.org/10.1007/s11032-016-0539-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Voorrips RE, Bink MCAM, Van de Weg WE (2012) PEDIMAP: software for the visualization of genetic and phenotypic data in pedigrees. J Heredity 103(6):903–907. https://doi.org/10.1093/jhered/ess060

    Article  Google Scholar 

  • van de Weg WE, Voorrips RE, Finkers R, Kodde LP, Jansen J, Bink MCAM (2004) Pedigree genotyping: a new pedigree-based approach of QTL identification and allele mining. Acta Hortic 663:45–50

    Google Scholar 

  • Whitaker VM, Hasing T, Chandler CK, Plotto A, Baldwin E (2011) Historical trends in strawberry fruit quality revealed by a trial of University of Florida cultivars and advanced selections. Hortscience 46:553–557

    Google Scholar 

  • Williams EB, Janick J, Emerson FH, Dayton DF, Mowry JB, Hough LF, et al. (1972) Six scab resistant apple selections released for grower testing. Purdue A.E.S. Res. Progress Rept.:399

  • Wu X, Blake S, Sleper DA, Shannon JG, Cregan P, Nguyen HT (2009) QTL, additive and epistatic effects for SCN resistance in PI 437654. Theor Appl Genet 118(6):1093–1105. https://doi.org/10.1007/s00122-009-0965-x

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to A. Peil (JKI Dresden, Germany), S. Tartarini (DCA Bologna, Italy) and G. Fazio of the USDA-ARS Plant Genetic Resources Unit at Geneva (NY, USA) for providing part of, respectively, the budwood of the individuals used in this study and freeze-dried leaves of a series of individuals that allowed the reconstruction of the pedigree of ‘Enterprise’. H. Muranty (INRA-Angers, France) is acknowledged for tracing the true historic pedigree data of the INRA selection X-6398. The authors also thank the INRA Experimental Unit (UE Horticole) for maintaining the IW populations in the field.

Funding

The research was partially funded by the ZUEFOS II Project (Züchtung feuerbrandtoleranter Obstsorten) of the Federal Office for Agriculture (FOAG, Switzerland). This work has also been partly funded under the EU Seventh Framework Program by the FruitBreedomics project no. 265582: Integrated Approach for increasing breeding efficiency in fruit tree crops.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Patocchi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van de Weg, E., Di Guardo, M., Jänsch, M. et al. Epistatic fire blight resistance QTL alleles in the apple cultivar ‘Enterprise’ and selection X-6398 discovered and characterized through pedigree-informed analysis. Mol Breeding 38, 5 (2018). https://doi.org/10.1007/s11032-017-0755-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-017-0755-0

Keywords

Navigation