Tree Genetics & Genomes

, 12:20 | Cite as

Genetic architecture of apple fruit quality traits following storage and implications for genetic improvement

  • Craig M. Hardner
  • Kate Evans
  • Chris Brien
  • Fred Bliss
  • Cameron Peace
Original Article
Part of the following topical collections:
  1. Breeding

Abstract

Accurate prediction of genetic potential and response to selection in breeding requires knowledge of genetic parameters for important selection traits. Data from breeding trials can be used to obtain estimates of these parameters so that predictions are directly relevant to the improvement program. Here, a factor allocation diagram was developed to describe the sampling design used to assess the quality of fresh and post-storage (2 months) fruit from advanced selection trial in an apple breeding program from which models for analyses were developed. Genetic variation was the largest source of variation for the fruit size, red colour type, proportion of red skin colour and lenticels, and instrumentally assessed fruit diameter, mass, puncture force and titratable acidity. In contrast, residual variation was the largest for fruit shape, juiciness, sweetness, aromatic flavour, eating and overall quality, and instrumental crispness. Genetic effects for traits were generally stable over fixed effects, except for a significant interaction with storage duration for firmness. Genetic correlations among traits were generally weak except between fruit mass (and diameter) and sensory size (0.98), titratable acidity and sensory acidity (0.97), puncture force and sensory firmness (0.96–0.90), crispness and juiciness (0.87), sweetness and aromatic flavour (0.84) and instrumental and sensory crispness (0.75). Predictions of the performance for seven commercial cultivars are presented. This study suggests that the Washington State apple production area can be treated as a single target environment and sufficient diversity exists to generate new elite cultivars. In addition, options for evaluating the efficiency of apple breeding are discussed.

Keywords

Heritability Repeatability Breeding Genetic correlation Cultivar testing 

References

  1. Abbott JA, Watada AE, Massie DR (1984) Sensory and instrument measurement of apple texture. J Am Soc Hortic Sci 109:221–228Google Scholar
  2. Alspach PA, Oraguzie N (2002) Estimation of genetic parameters of apple (Malus domestica) fruit quality from open-pollinated families. N Z J Crop Hortic Sci 30:219–228CrossRefGoogle Scholar
  3. Aprea E, Corollaro ML, Betta E, Endrizzi I, Dematte ML, Biasioli F, Gasperi F (2012) Sensory and instrumental profiling of 18 apple cultivars to investigate the relation between perceived quality and odour and flavour. Food Res Int 49:677–686CrossRefGoogle Scholar
  4. Baldwin EA, Goodner K, Plotto A (2008) Interaction of volatiles, sugars, and acids on perception of tomato aroma and flavor descriptors. J Food Sci 73:S294–S307CrossRefPubMedGoogle Scholar
  5. Bavay C, Symoneaux R, Maitre I, Kuznetsoya A, Brockhoff PB, Mehinagic E (2013) Importance of fruit variability in the assessment of apple quality by sensory evaluation. Postharvest Biol Technol 77:67–74CrossRefGoogle Scholar
  6. Bedford D (2001) Honeycrisp. Compact Fruit Tree 34:98–99Google Scholar
  7. Bonany J et al (2013) Consumer eating quality acceptance of new apple varieties in different European countries. Food Qual Prefer 30:250–259CrossRefGoogle Scholar
  8. Bonany J et al (2014) Preference mapping of apple varieties in Europe. Food Qual Prefer 32:317–329CrossRefGoogle Scholar
  9. Brennan JP, Kingwell RS, Thomson FM, Cullis BR (1998) Optimal strategies for regional cultivar testing. Aust J Agr Resour Econ 42:209–226CrossRefGoogle Scholar
  10. Brien CJ (1983) Analysis of variance tables based on experimental structure. Biometrics 39:53–59Google Scholar
  11. Brien CJ, Bailey RA (2006) Multiple randomizations. J R Stat Soc Ser B-Stat Methodol 68:571–599CrossRefGoogle Scholar
  12. Brien CJ, Demetrio CGB (2009) Formulating mixed models for experiments, including longitudinal experiments. J Agric Biol Environ Stat 14:253–280CrossRefGoogle Scholar
  13. Brien CJ, Harch BD, Correll RL, Bailey RA (2011) Multiphase experiments with at least one later laboratory phase I. Orthogonal designs. J Agric Biol Environ Stat 16:422–450CrossRefGoogle Scholar
  14. Brookfield PL, Nicoll S, Gunson FA, Harker FR, Wohlers M (2011) Sensory evaluation by small postharvest teams and the relationship with instrumental measurements of apple texture. Postharvest Biol Technol 59:179–186CrossRefGoogle Scholar
  15. Brown AG, Harvey DM (1971) Nature and inheritance of sweetness and acidity in cultivated apple. Euphytica 20:68CrossRefGoogle Scholar
  16. Bulmer MG (1971) Effect of selection on genetic variability. Am Nat 105:201–211CrossRefGoogle Scholar
  17. Chauvin MA, Ross CF, Pitts M, Kupferman E, Swanson B (2010) Relationship between instrumental and sensory determination of apple and pear texture. J Food Qual 33:181–198CrossRefGoogle Scholar
  18. Corollaro ML et al (2013) Sensory profiling of apple: methodological aspects, cultivar characterisation and postharvest changes. Postharvest Biol Technol 77:111–120CrossRefGoogle Scholar
  19. Corollaro ML et al (2014a) A combined sensory-instrumental tool for apple quality evaluation. Postharvest Biol Technol 96:135–144CrossRefGoogle Scholar
  20. Corollaro ML, Gasperi F, Grappadelli LC (2014b) An overview of sensory quality of apple fruit. Journal of the American Pomological Society 68:141–157Google Scholar
  21. Costa F et al (2005) Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus domestica Borkh). Euphytica 141:181–190CrossRefGoogle Scholar
  22. Costa F et al (2012) Texture dynamics during postharvest cold storage ripening in apple (Malus x domestica Borkh.). Postharvest Biol Technol 69:54–63CrossRefGoogle Scholar
  23. Daillant-Spinnler B, MacFie HJH, Beyts PK, Hedderley D (1996) Relationships between perceived sensory properties and major preference directions of 12 varieties of apples from the southern hemisphere. Food Qual Prefer 7:113–126CrossRefGoogle Scholar
  24. DeLacy IH, Basford KE, Cooper M, Bull JK, McLaren CG (1996) Analysis of multi-environment trials: an historical perspective. In: Cooper M, Hammer GL (eds) Plant adaptation and crop improvement. CAB International, Wallingford, pp 39–124Google Scholar
  25. Dever MC, Cliff MA, Hall JW (1995) Analysis of variation and multivariate relationships among analytical and sensory characteristics in whole apple evaluation. J Sci Food Agric 69:329–338CrossRefGoogle Scholar
  26. 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
  27. Echeverria G, Lara I, Fuentes T, Lopez ML, Graell J, Puy J (2004) Assessment of relationships between sensory and instrumental quality of controlled-atmosphere-stored ‘Fuji’ apples by multivariate analysis. J Food Sci 69:S368–S375CrossRefGoogle Scholar
  28. Echeverria G, Graell J, Lara I, Lopez ML, Puy J (2008) Panel consonance in the sensory evaluation of apple attributes: influence of mealiness on sweetness perception. J Sens Stud 23:656–670CrossRefGoogle Scholar
  29. Evans K (2013) Apple breeding in the Pacific Northwest. Eucarpia Fruit Breeding and Genetics. Acta Hortiuculturae 976:75–78CrossRefGoogle Scholar
  30. Evans K, Brutcher L, Konishi B, Barritt B (2010) Correlation of sensory analysis with physical textural data from a computerized penetrometer in the Washington State University Apple Breeding Program. HortTechnology 20:1026–1029Google Scholar
  31. Falconer DS, Mackay TFC (1996) An introduction to quantitative genetics, 4th edn. Longman, EssexGoogle Scholar
  32. Fellman JK, Rudell DR, Mattinson DS, Mattheis JP (2003) Relationship of harvest maturity to flavor regeneration after CA storage of ‘Delicious’ apples. Postharvest Biol Technol 27:39–51CrossRefGoogle Scholar
  33. Forde CG, Williams ER, O’Riordan PJ (2007) Use of multi-stratum design and analysis in a sensory trial. Food Qual Prefer 18:614–618CrossRefGoogle Scholar
  34. Gilmour AR, Gogel B, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel HempsteadGoogle Scholar
  35. Gitonga VW, Koning-Boucoiran CFS, Verlinden K, Dolstra O, Visser RGF, Maliepaard C, Krens FA (2014) Genetic variation, heritability and genotype by environment interaction of morphological traits in a tetraploid rose population. BMC Genet 15:32CrossRefGoogle Scholar
  36. Guan Y, Peace C, Rudell D, Verma S, Evans K (2015) QTLs detected for individual sugars and soluble solids content in apple. Mol Breed 35:1–13CrossRefGoogle Scholar
  37. Hahsler M, Hornik K, Buchta C (2008) Getting things in order: an introduction to the R package seriation. J Stat Softw 25:1–34CrossRefGoogle Scholar
  38. Hampson CR, McKenzie DL (2006) Sensory characteristics of 21 new apple cultivars after short-term cold air storage. Journal of the American Pomological Society 60:9–19Google Scholar
  39. Hampson CR, Quamme HA, Hall JW, MacDonald RA, King MC, Cliff MA (2000) Sensory evaluation as a selection tool in apple breeding. Euphytica 111:79–90CrossRefGoogle Scholar
  40. Hampson C et al (2007) Performance of apple cultivars in the 1999 NE-183 regional project planting III. Fruit sensory characteristics. Journal of the American Pomological Society 61:115–126Google Scholar
  41. 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 89:81–91CrossRefGoogle Scholar
  42. Harker FR, Maindonald J, Murray SH, Gunson FA, Hallett IC, Walker SB (2002a) Sensory interpretation of instrumental measurements 1: texture of apple fruit. Postharvest Biol Technol 24:225–239CrossRefGoogle Scholar
  43. Harker FR, Marsh KB, Young H, Murray SH, Gunson FA, Walker SB (2002b) Sensory interpretation of instrumental measurements 2: sweet and acid taste of apple fruit. Postharvest Biol Technol 24:241–250CrossRefGoogle Scholar
  44. Harker FR, Gunson FA, Jaeger SR (2003) The case for fruit quality: an interpretive review of consumer attitudes, and preferences for apples. Postharvest Biol Technol 28:333–347CrossRefGoogle Scholar
  45. Harker FR, Amos RL, Echeverria G, Gunson FA (2006) Influence of texture on taste: Insights gained during studies of hardness, juiciness, and sweetness of apple fruit. J Food Sci 71:S77–S82CrossRefGoogle Scholar
  46. Henderson CR (1975) Best linear unbiased estimation and prediction under a selection model. Biometrics 31:423–447CrossRefPubMedGoogle Scholar
  47. Henderson CR (1984) Applications of linear models in animal breeding. University of Guelph, GuelphGoogle Scholar
  48. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  49. Jackson JE (2003) Eating quality and its retention. In: Jackson JE (ed) The Biology of apples and pears. Cambridge University Press, Cambridge, pp 341–383Google Scholar
  50. Karlsen AM, Aaby K, Sivertsen H, Baardseth P, Ellekjaer MR (1999) Instrumental and sensory analysis of fresh Norwegian and imported apples. Food Qual Prefer 10:305–314CrossRefGoogle Scholar
  51. Kempton RA (1984) The use of biplots in interpreting variety by environment interactions. J Agric Sci 103:123–135CrossRefGoogle Scholar
  52. Kenis K, Keulemans J, Davey MW (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661Google Scholar
  53. Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997CrossRefPubMedGoogle Scholar
  54. King GJ et al (2000) Quantitative genetic analysis and comparison of physical and sensory descriptors relating to fruit flesh firmness in apple (Malus pumila Mill.). Theor Appl Genet 100:1074–1084CrossRefGoogle Scholar
  55. Kouassi AB et al (2009) Estimation of genetic parameters and prediction of breeding values for apple fruit-quality traits using pedigreed plant material in Europe. Tree Genet Genomes 5:659–672CrossRefGoogle Scholar
  56. Kuhn BF, Thybo AK (2001) Sensory quality of scab-resistant apple cultivars. Postharvest Biol Technol 23:41–50CrossRefGoogle Scholar
  57. 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 173:207–222CrossRefGoogle Scholar
  58. Kumar S, Volz R, 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 7:1079–1088CrossRefGoogle Scholar
  59. 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 14Google Scholar
  60. Land DG, Shepard R (1987) Scaling and ranking methods. In: Piggot J (ed) Sensory analysis of foods. Elsevier, New York, pp 155–185Google Scholar
  61. Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus×domestica Borkh.) genome. Theor Appl Genet 106:1497–1508Google Scholar
  62. Longhi S, Cappellin L, Guerra W, Costa F (2013) Validation of a functional molecular marker suitable for marker-assisted breeding for fruit texture in apple (Malus x domestica Borkh.). Mol Breed 32:841–852CrossRefGoogle Scholar
  63. Maliepaard C, Alston FH, 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 97:60–73Google Scholar
  64. McKay SJ, Bradeen JM, Luby JJ (2011) Prediction of genotypic values for apple fruit texture traits in a breeding population derived from ‘Honeycrisp’. J Am Soc Hortic Sci 136:408–414Google Scholar
  65. Meilgaard M, Civille GV, Carr BT (1999) Sensory evaluation techniques, 3rd edn. CRC, Boca RatonCrossRefGoogle Scholar
  66. Miller S et al (2004) Performance of apple cultivars in the 1995 NE-183 Regional Project planting: II. Fruit quality characteristics. Journal of the American Pomological Society 58:65–77Google Scholar
  67. Miller S et al (2005a) Performance of apple cultivars in the 1995 NE-183 Regional Project planting: III. Fruit sensory characteristics. Journal of the American Pomological Society 59:28–43Google Scholar
  68. Miller SS et al (2005b) Effect of cultivar and site on fruit quality as demonstrated by the NE-183 Regional Project on apple cultivars. HortTechnology 15:886–895Google Scholar
  69. Miller S et al (2007) Performance of apple cultivars in the 1999 NE-183 Regional Project planting II. Fruit quality characteristics. Journal of the American Pomological Society 61:97–114Google Scholar
  70. Mohr CL, Mohr BC (2000) Apple maturation state and condition determination method in plantation, involves determining position of plunger moved through data points in each zones of fruit, to compute data related to viscoelastic properties of fruit. US6643599-B1Google Scholar
  71. Munzel U, Bandelow B (1998) The use of parametric vs. nonparametric tests in the statistical evaluation of rating scales. Pharmacopsychiatry 31:222–224CrossRefPubMedGoogle Scholar
  72. Murray JM, Delahunty CM, Baxter IA (2001) Descriptive sensory analysis: past, present and future. Food Res Int 34:461–471CrossRefGoogle Scholar
  73. Nybom N (1959) On the inheritance of acidity in cultivated apples. Hereditas 45:332–350CrossRefGoogle Scholar
  74. Nybom H, Afzadi MA, Sehic J, Hertog M (2013) DNA marker-assisted evaluation of fruit firmness at harvest and post-harvest fruit softening in a diverse apple germplasm. Tree Genet Genomes 9:279–290CrossRefGoogle Scholar
  75. Oraguzie NC, Hofstee ME, Brewer LR, Howard C (2001) Estimation of genetic parameters in a recurrent selection program in apple. Euphytica 118:29–37CrossRefGoogle Scholar
  76. 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 x domestica Borkh.). Theor Appl Genet 108:1526–1533CrossRefPubMedGoogle Scholar
  77. Oraguzie N, Alspach P, Volz R, Whitworth C, Ranatunga C, Weskett R, Harker R (2009) Postharvest assessment of fruit quality parameters in apple using both instruments and an expert panel. Postharvest Biol Technol 52:279–287CrossRefGoogle Scholar
  78. Patterson HD, Thompson R (1971) Recovery of interblock information when block sizes are unequal. Biometrika 58:545–554CrossRefGoogle Scholar
  79. Piepho HP (1997) Analyzing genotype-environment data by mixed models with multiplicative terms. Biometrics 53:761–766CrossRefGoogle Scholar
  80. Piepho HP, Mohring J, Williams ER (2013) Why randomize agricultural experiments? J Agron Crop Sci 199:374–383CrossRefGoogle Scholar
  81. Pitts M, Drake S, Cavalieri R (1997) Apple size and length of storage affects firmness. http://postharvest.tfrec.wsu.edu/pages/PC97D. Accessed 07 Aug 2014
  82. Seppa L, Peltoniemi A, Tahvonen R, Tuorila H (2013) Flavour and texture changes in apple cultivars during storage. Lwt-Food Science and Technology 54:500–512CrossRefGoogle Scholar
  83. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591CrossRefGoogle Scholar
  84. Smith A, Cullis B, Thompson R (2001) Analyzing variety by environment data using multiplicative mixed models and adjustments for spatial field trend. Biometrics 57:1138–1147CrossRefPubMedGoogle Scholar
  85. Stram DO, Lee JW (1994) Variance-components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177CrossRefPubMedGoogle Scholar
  86. Sunako T, Sakuraba W, Senda M, Akada S, Ishikawa R, Niizeiki M, Harada T (1999) An allele of the ripening-specific 1-aminocyclopropane-1-carboxylic acid synthase gene (ACS1) in apple fruit with a long storage life. Plant Phys 119:1297–1304Google Scholar
  87. Thompson R, Cullis B, Smith A, Gilmour A (2003) A sparse implementation of the average information algorithm for factor analytic and reduced rank variance models. Aust N Z J Stat 45:445–459CrossRefGoogle Scholar
  88. Visser T, Verhaegh JJ (1978) Inheritance and selection of some fruit characteristics of apple. 1. Inheritance of low and high acidity. Euphytica 27:753–760CrossRefGoogle Scholar
  89. Wilkinson RI et al (2008) Effects of 1-methylcyclopropene on firmness and flesh browning in Pink Lady (TM) apples. Journal of Horticultural Science & Biotechnology 83:165–170CrossRefGoogle Scholar
  90. Wilks SS (1938) The large-sample distribution of the likelihood ratio for testing composite hypotheses. Ann Math Stat 9:60–62CrossRefGoogle Scholar
  91. Williams ER, Matheson AC, Harwood CE (2002) Experimental design and analysis for tree improvement. CSIRO Publishing, MelbourneGoogle Scholar
  92. Yates F (1936) A new method of arranging variety trials involving a large number of varieties. J Agric Sci 26:424–455Google Scholar
  93. Zhu YM, 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 4:555–562CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Craig M. Hardner
    • 1
  • Kate Evans
    • 2
  • Chris Brien
    • 3
  • Fred Bliss
    • 4
  • Cameron Peace
    • 5
  1. 1.Queensland Alliance for Agriculture and Food InnovationUniversity of QueenslandSt LuciaAustralia
  2. 2.Washington State University (WSU-TFREC)WenatcheeUSA
  3. 3.University of South AustraliaAdelaideAustralia
  4. 4.Department of Plant SciencesUniversity of CaliforniaDavisUSA
  5. 5.Department of HorticultureWashington State UniversityPullmanUSA

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