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Identification and stability of QTLs for fruit quality traits in apple

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Abstract

Breeding for fruit quality traits is complex due to the polygenic (quantitative) nature of the genetic control of these traits. Therefore, to improve the speed and efficiency of genotype selection, attention in recent years has focused on the identification of quantitative trait loci (QTLs) and molecular markers associated with these QTLs. However, despite the huge potential of molecular markers in breeding programmes, their implementation in practice has been limited by the lack of information on the stability of QTLs across different environments and within different genetic backgrounds. Here, we present the results from a comprehensive analysis of the inheritance of fruit quality traits within a population derived from a cross between the apple cultivars ‘Telamon’ and ‘Braeburn’ over two successive seasons. A total of 74 different QTLs were identified for all the major fruit physiological traits including fruit height, diameter, weight and stiffness, flesh firmness, rate of flesh browning, acidity, the ºBrix content and harvest date. Seventeen of these QTLs were ‘major’ QTLs, accounting for over 20% of the observed population variance of the trait. However, only one third (26) of the identified QTLs were stable over both harvest years, and of these year-stable QTLs only one was a major QTL. A direct comparison with published QTL results obtained using other populations (King et al., Theor Appl Genet 102:1227–1235, 2001; Liebhard et al., Plant Mol Biol 52:511–526, 2003) is difficult because the linkage maps do not share a sufficient number of common markers and due to differences in the trait evaluation protocols. Nonetheless, our results suggest that for the six fruit quality traits which were measured in all populations, nine out of a total of 45 QTLs were common or stable across all population × environments combinations. These results are discussed in the framework of the development and application of molecular markers for fruit quality trait improvement.

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References

  • Bortiri E, Jackson D, Hake S (2006) Advances in maize genomics: the emergence of positional cloning. Curr Opin Plant boil 9:164–171

    Article  CAS  Google Scholar 

  • Bouchez A, Hospital F, Causse M, Gallais A, Charcosset A (2002) Marker-assisted introgression of favorable alleles at quantitative trait loci between maize elite lines. Genetics 162:1945–1959

    PubMed  CAS  Google Scholar 

  • Causse M, Saliba-Colombani V, Lecomte L, Duffe P, Rousselle P, Buret M (2002) QTL analysis of fruit quality in fresh market tomato: a few chromosome regions control the variation of sensory and instrumental traits. J Exp Bot 53:2089–2098

    Article  PubMed  CAS  Google Scholar 

  • Chaïb J, Lecomte L, Buret M, Causse M (2006) Stability over genetic backgrounds, generations and years of quantitative trait locus (QTLs) for organoleptic quality in tomato. Theor Appl Genet 112(5):934–944

    Article  PubMed  Google Scholar 

  • Chen H, de Baerdemaeker J (1993) Effect of apple shape on acoustic measurements of firmness. J Agric Eng Res 56:259–266

    Article  Google Scholar 

  • Cisneros-Zevallos L (2003) The use of controlled postharvest abiotic stresses as a tool for enhancing the nutraceutical content and adding-value of fresh fruits and vegetables. J Food Sci 68:1560–1565

    Article  CAS  Google Scholar 

  • Costa F, Stella S, Van de Weg WE, Guerra W, Cecchinel M, Dallavia J, Koller B, Sansavini S (2005) Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus domestica Borkh). Euphytica 141:181–190

    Article  CAS  Google Scholar 

  • Davey MW, Keulemans J (2004) Determining the potential to breed for enhanced antioxidant status in Malus: Mean inter- and intravarietal fruit vitamin C and glutathione contents at harvest and their evolution during storage. J Agric Food Chem 52:8031–8038

    Article  PubMed  CAS  Google Scholar 

  • Davey MW, Van Montagu M, Inze D, Sanmartin M, Kanellis A, Smirnoff N, Benzie IJJ, Strain JJ, Favell D, Fletcher J (2000) Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860

    Article  CAS  Google Scholar 

  • Davey MW, Kenis K, Keulemans J (2006) Genetic control of fruit vitamin C contents. Plant Physiol 142:343–351

    Article  PubMed  CAS  Google Scholar 

  • Davey MW, Auwerkerken A, Keulemans J (2007) Relationship of apple vitamin C and antioxidant contents to harvest date and postharvest pathogen infection. J Sci Food Agric 87:802–813

    Article  CAS  Google Scholar 

  • Etienne C, Rothan C, Moing A, Plomion C, Bodenes C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159

    Article  PubMed  CAS  Google Scholar 

  • Ferguson I, Volz R, Woolf A (1999) Preharvest factors affecting physiological disorders of fruit. Postharvest Biol Technol 15:255–262

    Article  Google Scholar 

  • Franck C, Baetens M, Lammertyn J, Scheerlinck N, Davey MW, Nikolai BM (2003a) Ascorbic acid mapping to study core breakdown development in ‘Conference’ pears. Postharvest Biol Technol 30:133–142

    Article  CAS  Google Scholar 

  • Franck C, Baetens M, Lammertyn J, Verboven P, Davey MW, Nicolai BM (2003b) Ascorbic acid concentration in cv. conference pears during fruit development and postharvest storage. J Agric Food Chem 51:4757–4763

    Article  PubMed  CAS  Google Scholar 

  • Gong YP, Toivonen PMA, Lau OL, Wiersma PA (2001) Antioxidant system level in ‘Braeburn’ apple is related to its browning disorder. Bot Bull Acad Sinica 42:259–264

    CAS  Google Scholar 

  • Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A (2004) Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor Appl Genet 109:1702–1709

    Article  PubMed  CAS  Google Scholar 

  • Hodges DM, Lester GE, Munro KD, Toivonen PMA (2004) Oxidative stress: importance for postharvest quality. Hortscience 39:924–929

    CAS  Google Scholar 

  • Honda C, Kotoda N, Wada M, Kondo S, Kobayashi S, Soejima J, Zhang ZL, Tsuda T, Moriguchi T (2002) Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol Biochem 40:955–962

    Article  CAS  Google Scholar 

  • Kenis K, Keulemans J (2005) Genetic linkage maps of two apple cultivars (Malus x domestica Borkh.) based on AFLP and microsatellite markers. Mol Breed 15:205–219

    Article  CAS  Google Scholar 

  • Kenis K, Keulemans J (2007) Study of tree architecture of apple (Malus x domestica Borkh.) by QTL analysis of growth traits. Mol Breed 19:193–208

    Article  CAS  Google Scholar 

  • King GJ, Maliepaard C, Lynn JR, Alston FH, Durel CE, Evans KM, Griffon B, Laurens F, Manganaris AG, Schrevens T, 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

    Article  Google Scholar 

  • King GJ, Lynn JR, Dover CJ, Evans KM, Seymour GB (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

    Article  CAS  Google Scholar 

  • Lauri PE, Lespinasse JM (1993) The relationship between cultivar fruiting type and fruiting branch characteristics in apple trees. Acta Hort 349:259–296

    Google Scholar 

  • Lecomte L, Duffe P, Buret M, Servin B, Hospital F, Causse M (2004) Marker-assisted introgression of five QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. Theor Appl Genet 109:658–668

    Article  PubMed  CAS  Google Scholar 

  • 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 x domestica Borkh.). Mol Breed 10:217–241

    Article  CAS  Google Scholar 

  • Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003a) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526

    Article  PubMed  CAS  Google Scholar 

  • Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003b) Creating a saturated reference map for the apple (Malus x domestica Borkh.) genome. Theor Appl Genet 106:1497–1508

    PubMed  CAS  Google Scholar 

  • Liebhard R, Koller B, Patocchi A, Kellerhals M, Pfammatter W, Jermini M, Gessler C (2003c) Mapping quantitative field resistance against apple scab in a ‘Fiesta’ × ‘Discovery’ progeny. Phytopathology 93:493–501

    Article  Google Scholar 

  • 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 97:60–73

    Article  CAS  Google Scholar 

  • Masood MS, Seiji Y, Shinwari ZK, Anwar R (2004) Mapping quantitative trait loci (QTLS) for salt tolerance in rice (Oryza sativa) using RFLPs. Pak J Bot 36:825–834

    Google Scholar 

  • Merzlyak MN, Solovchenko AE, Chivkunova OB (2002) Patterns of pigment changes in apple fruits during adaptation to high sunlight and sunscald development. Plant Physiol Biochem 40:679–684

    Article  CAS  Google Scholar 

  • Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk YK (2006) Analyses of expressed sequence tags from apple. Plant Physiol 141:147–166

    Article  PubMed  Google Scholar 

  • Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD (1991) Mendelian factors underlying quantitative traits in tomato—comparison across species, generations, and environments. Genetics 127:181–197

    PubMed  CAS  Google Scholar 

  • Patocchi A, Walser M, Tartarini S, Broggini GAL, Gennari F, Sansavini S, Gessler C (2005) Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630–636

    Article  PubMed  CAS  Google Scholar 

  • Quilot B, Wu BH, Kervella J, Genard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897

    Article  PubMed  CAS  Google Scholar 

  • Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408

    Article  PubMed  CAS  Google Scholar 

  • Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, Willmitzer L, Zamir D, Fernie AR (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454

    Article  PubMed  CAS  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 2:202–224

    Article  Google Scholar 

  • Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630

    Article  PubMed  CAS  Google Scholar 

  • Stangoulis JCR, Huynh BL, Welch RM, Choi EY, Graham RD (2007) Quantitative trait loci for phytate in rice grain and their relationship with grain micronutrient content. Euphytica 154:289–294

    Article  Google Scholar 

  • Treutter D (2001) Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul 34:71–89

    Article  CAS  Google Scholar 

  • Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0; Software for the calculation of QTL positions on genetic maps. Plant Research International B.V., Wageningen

    Google Scholar 

  • Vinatzer BA, Patocchi A, Tartarini S, Gianfranceschi L, Sansavini S, Gessler C (2004) Isolation of two microsatellite markers from BAC clones of the Vf scab resistance region and molecular characterization of scab-resistant accessions in Malus germplasm. Plant Breed 123:321–326

    Article  CAS  Google Scholar 

  • Vinod MS, Sharma N, Manjunatha K, Kanbar A, Prakash NB, Shashidhar HE (2006) Candidate genes for drought tolerance and improved productivity in rice (Oryza sativa L.). J Biosci 31:69–74

    Article  PubMed  CAS  Google Scholar 

  • Wan XY, Wan JM, Jiang L, Wang JK, Zhai HQ, Weng JF, Wang HL, Lei CL, Wang JL, Zhang X, Cheng ZJ, Guo XP (2006) QTL analysis for rice grain length and fine mapping of an identified QTL with stable and major effects. Theor Appl Genet 112:1258–1270

    Article  PubMed  CAS  Google Scholar 

  • Woolf AB, Ferguson IB (2000) Postharvest responses to high fruit temperatures in the field. Postharvest Biol Technol 21:7–20

    Article  Google Scholar 

  • Wunsche JN, Lakso AN (2000) The relationship between leaf area and light interception by spur and extension shoot leaves and apple orchard productivity. Hortscience 35:1202–1206

    Google Scholar 

  • Wunsche JN, Lakso AN, Robinson TL, Lenz F, Denning SS (1996) The bases of productivity in apple production systems: the role of light interception by different shoot types. J Am Soc Hortic Sci 121:886–893

    Google Scholar 

  • Wunsche JN, Greer DH, Laing WA, Palmer JW (2005) Physiological and biochemical leaf and tree responses to crop load in apple. Tree Physiol 25:1253–1263

    PubMed  CAS  Google Scholar 

  • Xu ML, Huaracha E, Korban SS (2001) Development of sequence-characterized amplified regions (SCARs) from amplified fragment length polymorphism (AFLP) markers tightly linked to the Vf gene in apple. Genome 44:63–70

    Article  PubMed  CAS  Google Scholar 

  • Xu JL, Lafitte HR, Gao YM, Fu BY, Torres R, Li ZK (2005) QTLs for drought escape and tolerance identified in a set of random introgression lines of rice. Theor Appl Genet 111:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Yoon DB, Kang KH, Kim HJ, Ju HG, Kwon SJ, Suh JP, Jeong OY, Ahn SN (2006) Mapping quantitative trait loci for yield components and morphological traits in an advanced backcross population between Oryza grandiglumis and the O. sativa japonica cultivar Hwaseongbyeo. Theor Appl Genet 112:1052–1062

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was carried out within the framework of a post-doctoral fellowship for Katrien Kenis funded by ‘Instituut voor de aanmoediging van Innovatie door Wetenschap en Technologie in Vlaanderen’ (I.W.T.). The contribution of Otto van Poeselaere and Eva A. Davey in the preparation of this manuscript is gratefully acknowledged.

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Authors and Affiliations

  1. Laboratory of Fruit Breeding and Biotechnology, Department Crop Biotechnics, Catholic University of Leuven, W. De Croylaan 42, 3001, Heverlee, Belgium

    Katrien Kenis & Johan Keulemans

  2. Centre for Fruit Culture, Leuven Research and Development Division, Catholic University of Leuven, Willem de Croylaan 42, 3001, Heverlee, Belgium

    Mark W. Davey

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  1. Katrien Kenis
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  2. Johan Keulemans
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  3. Mark W. Davey
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Correspondence to Mark W. Davey.

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Communicated by P. Arús.

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Kenis, K., Keulemans, J. & Davey, M.W. Identification and stability of QTLs for fruit quality traits in apple. Tree Genetics & Genomes 4, 647–661 (2008). https://doi.org/10.1007/s11295-008-0140-6

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  • DOI: https://doi.org/10.1007/s11295-008-0140-6

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