Skip to main content
SpringerLink
Log in

Identification and validation of a QTL influencing bitter pit symptoms in apple (Malus × domestica)

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Bitter pit is one of the most economically important physiological disorders affecting apple fruit production, causing soft discrete pitting of the cortical flesh of the apple fruits which renders them unmarketable. The disorder is heritable; however, the environment and cultural practices play a major role in expression of symptoms. Bitter pit has been shown to be controllable to a certain extent using calcium sprays and dips; however, their use does not entirely prevent the incidence of the disorder. Previously, bitter pit has been shown to be controlled by two dominant genes, and markers on linkage group 16 of the apple genome were identified that were significantly associated with the expression of bitter pit symptoms in a genome-wide association study. In this investigation, we identified a major QTL for bitter pit defined by two microsatellite (SSR) markers. The association of the SSRs with the bitter pit locus, and their ability to predict severe symptom expression, was confirmed through screening of individuals with stable phenotypic expression from an additional mapping progeny. The data generated in this current study suggest a two gene model could account for the control of bitter pit symptom expression; however, only one of the loci was detectable, most likely due to dominance of alleles carried by both parents of the mapping progeny used. The SSR markers identified are cost-effective, robust and multi-allelic and thus should prove useful for the identification of seedlings with resistance to bitter pit using marker-assisted selection in apple breeding programs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen GJ, Chu SP, Harrington CL et al (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Amarante CVT, Chaves DV, Ernani PR (2006) Mineral composition and bitter pit severity in ‘Catarina’ apples. Rev Bras Frutic 28:51–54

    Article  Google Scholar 

  • Amarante CVT, Miqueloto A, Steffens CA, Santos A, Argenta LC (2013) Changes in xylem functionality during apple fruit development: implications on calcium concentration and incidence of bitter pit. Acta Hortic 1012:135–140

    Google Scholar 

  • Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52

    Article  CAS  PubMed  Google Scholar 

  • Blatt MR (2004) Membrane transport in plants. Blackwell Publishing, Oxford

    Google Scholar 

  • Chagne D, Crowhurst RN, Troggio M et al (2012) Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One 7:12

    Article  Google Scholar 

  • Chen DH, Ronald PC (1999) A rapid DNA minipreparation method suitable for AFLP and other PCR applications. Plant Mol Biol Rep 17:53–57

    Article  CAS  Google Scholar 

  • Delong WA (1936) Variations in the chief ash constituents of apples affected with blotchy cork. Plant Physiol 11:453–456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • DeLong JM, Prange RK, Harrison PA (2004) The influence of pre-storage delayed cooling on quality and disorder incidence in ‘Honeycrisp’ apple fruit. Postharvest Biol Technol 33:175–180

    Article  Google Scholar 

  • Evans K (2013) Apple breeding in the Pacific Northwest. Acta Hortic 976:75–78

    Google Scholar 

  • Fallahi E, Conway WS, Hickey KD, Sams CE (1997) The role of calcium and nitrogen in postharvest quality and disease resistance of apples. HortScience 32:831–835

    CAS  Google Scholar 

  • Faust M, Shear CB (1968) Corking disorders of apples: a physiological and biochemical review. Bot Rev 34:441–469

    Article  Google Scholar 

  • Ferguson IB, Watkins CB (1989) Bitter pit in apple fruit. Hortic Rev 11:289–355

    CAS  Google Scholar 

  • Fernandez-Fernandez F, Evans KM, Clarke JB, Govan CL, James CM, Maric S, Tobutt KR (2008) Development of an STS map of an interspecific progeny of Malus. Tree Genet Genomes 4:469–479

    Article  Google Scholar 

  • Fernandez-Fernandez F, Antanaviciute L, Govan CL, Sargent DJ (2011) Development of a multiplexed microsatellite set for fingerprinting red raspberry (Rubus idaeus) germplasm and its transferability to other Rubus species. J Berry Res 1:177–187

    CAS  Google Scholar 

  • Fernandez-Fernandez F, Antanaviciute L, van Dyk MM, Tobutt KR, Evans KM, Rees DJG, Dunwell JM, Sargent DJ (2012) A genetic linkage map of an apple rootstock progeny anchored to the Malus genome sequence. Tree Genet Genomes 8:991–1002

    Article  Google Scholar 

  • Greene DW (1991) Reduced rates and multiple sprays of paclobutrazol control growth and improve fruit quality of delicious apples. J Am Soc Hortic Sci 116:807–812

    CAS  Google Scholar 

  • Hamilton DWA, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hewett EW, Watkins CB (1991) Bitter pit control by sprays and vacuum infiltration of calcium in ‘Cox’s Orange Pippin’ apples. HortScience 26:284–286

    CAS  Google Scholar 

  • Korban SS, Swiader JM (1984) Genetic and nutritional status in bitter pit-resistant and pit-susceptible apple seedlings. J Am Soc Hortic Sci 109:428–432

    CAS  Google Scholar 

  • Kumar S, Garrick DJ, Bink M, Whitworth C, Chagne D, Volz RK (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics 14:13

    Article  Google Scholar 

  • Lewis TL (1980) Rate of uptake and longitudinal distribution of potassium, calcium and magnesium in the flesh of developing apple fruits of 9 cultivars. J Hortic Sci 55:57–63

    CAS  Google Scholar 

  • Lotze E, Theron KI (2006) Dynamics of calcium uptake with pre-harvest sprays to reduce bitter pit in ‘Golden Delicious’. Acta Hortic 721:313–319

    CAS  Google Scholar 

  • Lotze E, Joubert J, Theron KI (2008) Evaluating pre-harvest foliar calcium applications to increase fruit calcium and reduce bitter pit in ‘Golden Delicious’ apples. Sci Hortic 116:299–304

    Article  Google Scholar 

  • Maliepaard C, Alston FH, van Arkel G et al (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73

    Article  CAS  Google Scholar 

  • Miqueloto A, do Amarante CVT, Steffens CA, dos Santos A, Mitcham E (2014) Relationship between xylem functionality, calcium content and the incidence of bitter pit in apple fruit. Sci Hortic 165:319–323

    Article  CAS  Google Scholar 

  • Padmarasu S, Sargent DJ, Jaensch M, Kellerhals M, Tartarini S, Velasco R, Troggio M, Patocchi A (2014) Fine-mapping of the apple scab resistance locus Rvi12 (Vb) derived from ‘Hansen’s baccata #2’. Mol Breed 34:2119–2129. doi:10.1007/s11032-014-0167-3

  • Pavicic N, Jemric T, Kurtanjek Z, Cosic T, Pavlovic I, Blaskovic D (2004) Relationship between water-soluble Ca and other elements and bitter pit occurrence in ‘Idared’ apples: a multivariate approach. Ann Appl Biol 145:193–196

    Article  CAS  Google Scholar 

  • Perring MA, Pearson K (1986) Incidence of bitter pit in relation to the calcium content of apples—calcium distribution in the fruit. J Sci Food Agric 37:709–718

    Article  CAS  Google Scholar 

  • Pesis E, Ebeler SE, de Freitas ST, Padda M, Mitcham EJ (2010) Short anaerobiosis period prior to cold storage alleviates bitter pit and superficial scald in Granny Smith apples. J Sci Food Agric 90:2114–2123

    CAS  PubMed  Google Scholar 

  • Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100

    Article  CAS  PubMed  Google Scholar 

  • Sargent DJ, Passey T, Surbanovski N, Girona EL, Kuchta P, Davik J, Harrison R, Passey A, Whitehouse AB, Simpson DW (2012) A microsatellite linkage map for the cultivated strawberry (Fragaria × ananassa) suggests extensive regions of homozygosity in the genome that may have resulted from breeding and selection. Theor Appl Genet 124:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Schlotterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365–371

    Article  CAS  PubMed  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 × domestica Borkh.) genome. Tree Genet Genomes 2:202–224

    Article  Google Scholar 

  • Smock RM, Neubert AM (1950) Apples and apple products. Interscience Pub, New York

    Google Scholar 

  • Toth G, Gaspari Z, Jurka J (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V., Wageningen

    Google Scholar 

  • Van Ooijen JW (2009) MapQTL® 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B.V., Wageningen

    Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–841

    Article  CAS  PubMed  Google Scholar 

  • Volz RK, Alspach PA, Fletcher DJ, Ferguson IB (2006) Genetic variation in bitter pit and fruit calcium concentrations within a diverse apple germplasm collection. Euphytica 149:1–10

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Wang A, Brown S (2012) Genetic characterization of the Ma locus with pH and titratable acidity in apple. Mol Breed 30:899–912

    Article  CAS  Google Scholar 

  • Yuri JA, Retamales JB, Moggia C, Vasquez JL (2002) Bitter pit control in apples cv. Braeburn through foliar sprays of different calcium sources. Acta Hortic 594:453–460

    CAS  Google Scholar 

  • Zupan A, Mikulic-Petkovsek M, Cunja V, Stampar F, Veberic R (2013) Comparison of phenolic composition of healthy apple tissues and tissues affected by bitter pit. J Agric Food Chem 61:12066–12071

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Autonomous Province of Trento to the Fondazione Edmund Mach, Trentino, Italy.

Author information

Authors and Affiliations

  1. Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010, San Michele all’Adige, Italy

    M. Buti, L. Poles, D. Caset, P. Magnago, R. Velasco & D. J. Sargent

  2. East Malling Research, New Road, East Malling, Kent, ME19 6BJ, UK

    F. Fernandez Fernandez

  3. Natural Resources Institute, University of Greenwich, Chatham, Kent, ME4 4TB, UK

    R. J. Colgan

Authors
  1. M. Buti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Poles
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Caset
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Magnago
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Fernandez Fernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. J. Colgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Velasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. D. J. Sargent
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. J. Sargent.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11032_2015_258_MOESM1_ESM.tif

Supplementary Fig. 1 – Initial linkage map and QTL analysis using interval mapping for 94 individuals of R × X mapping population. Marker positions are given in cM, and accompanying graphs give LOD scores associated with bitter pit symptom expression.(TIFF 960 kb)

11032_2015_258_MOESM2_ESM.tif

Supplementary Fig. 2 – Schematic representation of the segregation of alleles within the R × X progeny and their associated expected phenotypes, according to the two gene model for bitter pit susceptibility of Korban and Swiader (1984). (TIFF 59 kb)

11032_2015_258_MOESM3_ESM.pdf

Supplementary Table 1 – Results of mapping and QTL analysis using interval mapping on a subset (n = 94) of the R × X mapping population that displayed a consistent phenotype across all three years of evaluation. The position of each of the nine markers across the linkage group is given, along with the LOD score and associated percentage variance explained for each marker. (PDF 14 kb)

11032_2015_258_MOESM4_ESM.pdf

Supplementary Table 2 – Results of mapping and QTL analysis using interval mapping the full mapping progeny of n = 364 individuals of the R × X mapping population across all three years of evaluation. The position of each marker across the linkage group is given, along with the LOD score and associated percentage variance explained for each of the four markers scored. (PDF 14 kb)

11032_2015_258_MOESM5_ESM.pdf

Supplementary Table 3 – Validation of alleles in coupling with severe bitter pit symptom expression in nine susceptible (phenotype 4) and seven resistant (phenotype 0) plants belonging to B × C progeny that gave a consistent phenotype over two years evaluation. (PDF 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buti, M., Poles, L., Caset, D. et al. Identification and validation of a QTL influencing bitter pit symptoms in apple (Malus × domestica). Mol Breeding 35, 29 (2015). https://doi.org/10.1007/s11032-015-0258-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-015-0258-9

Keywords

Search

Navigation