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Tree Genetics & Genomes

, 11:819 | Cite as

MetaQTL analysis provides a compendium of genomic loci controlling fruit quality traits in apple

  • Fabrizio CostaEmail author
Original Paper

Abstract

Fruit quality represents an important aspect of any fruit species, due to its economical importance and direct impact on consumers’ appreciation. In order to generate a compendium about the genomic intervals putatively involved in the control of the several fruit quality components, a Meta-quantitative trait loci (QTL) analysis was performed starting from a QTL mapping survey individually conducted on four full-sib populations. These progenies were simultaneously genotyped with 1289 SNP markers, of which 52 % were in common for at least two maps. The combination of the genotypic and phenotypic datasets allowed the identification of 56 QTLs, which were subsequently projected into a consensus map, reducing the total number of genomic intervals to 27 MetaQTLs. The majority of these regions, associated to fruit quality traits such as fruit skin color and flesh firmness, resulted also consistent with previous reports presented to date to the scientific community. This MetaQTL overview would represents a valuable source for genome anchoring and data mining investigation, suitable for a further in silico identification of relevant causal genes. As example is reported the case of Md-PG1, a gene known to control fruit firmness in apple and retrieved within the confidence interval of a MetaQTL associated to fruit firmness.

Keywords

MetaQTL  QTL mapping Apple Fruit quality Consensus map 

Notes

Acknowledgments

This research was supported by the post-Doc project CANDI-HAP founded by the Autonomous Province of Trento. The author wants to thank also Pierluigi Magnago and his team for plant maintenance, Livio Fadanelli for apple storage, and Massimo Pindo for the SNP genotyping facility.

Data Archiving Statement

Information about the SNP markers used in this work are available at the Genome Database for Rosaceae (GDR: www.rosaceae.org).

Supplementary material

11295_2014_819_MOESM1_ESM.doc (46 kb)
Suppl. Fig. 1 Trait distribution for fruit weight (panel B, D, F, H) and fruit firmness at harvest (panel A; C; E; G) assessed for the four populations: ‘FD’ (A and B panel), ‘FPL’ (C and D), ‘GDS’ (E and F) and ‘GDB’ (G and H). For each panel, the y-axes indicate the number of observations. The x-axes reports, instead, the kgcm−2 and the g for fruit firmness and weight, respectively. On each distribution the position of the parental cultivars is shown by arrows, while the black line indicates the best-fit line (DOC 46 kb)
11295_2014_819_MOESM2_ESM.ppt (158 kb)
Suppl. Fig. 2 Genetic alignment between the four individual maps (‘FD’, ‘FPL’ ‘GDS’ and ‘GDB’) and the consensus (CONS). In the figure the comparison of LG 3, 6, 11 and 16 is shown (PPT 158 kb)
11295_2014_819_MOESM3_ESM.ppt (316 kb)
Suppl. Fig. 3 QTL mapping confidence interval of ‘Fuji’ x ‘Delearly’ (‘FD’) (PPT 315 kb)
11295_2014_819_MOESM4_ESM.ppt (100 kb)
Suppl. Fig. 4 QTL mapping confidence interval of ‘Fuji’ x ‘Cripps Pink’ (‘FPL’) (PPT 100 kb)
11295_2014_819_MOESM5_ESM.ppt (123 kb)
Suppl. Fig. 5 QTL mapping confidence interval of ‘Golden Delicious’ x ‘Scarlet’ (‘GDS’) (PPT 123 kb)
11295_2014_819_MOESM6_ESM.ppt (110 kb)
Suppl. Fig. 6 QTL mapping confidence interval of ‘Golden Delicious’ x ‘Braeburn’ (‘GDB’) (PPT 110 kb)
11295_2014_819_MOESM7_ESM.docx (56 kb)
Suppl. Table 1 QTL mapping survey for the ‘Fuji’ x ‘Delearly’ population. For each trait the linkage groups where the QTL was identified (LG), the LOD value (LOD), the percentage of variance explained by the QTL (R2) and the marker close to the QTL peak (Marker) is reported (DOCX 55 kb)
11295_2014_819_MOESM8_ESM.docx (49 kb)
Suppl. Table 2 QTL mapping survey for the ‘Fuji’ x ‘Cripps Pink’ population. The description of the table is the same as for Suppl. Table 1 (DOCX 49 kb)
11295_2014_819_MOESM9_ESM.docx (52 kb)
Suppl. Table 3 QTL mapping survey for the ‘Golden Delicious’ x ‘Scarlet’ population. The description of the table is the same as for Suppl. Table 1 (DOCX 51 kb)
11295_2014_819_MOESM10_ESM.docx (39 kb)
Suppl. Table 4 QTL mapping survey for the ‘Golden Delicious’ x ‘Braeburn’ population. The description of the table is the same as for Suppl. Table 1. (DOCX 388 kb)
11295_2014_819_MOESM11_ESM.docx (29 kb)
Suppl. Table 5 QTL model computed in order to define the number of MetaQTL per each LG (DOCX 28 kb)

References

  1. Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad 76:170–174CrossRefGoogle Scholar
  2. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055CrossRefPubMedGoogle Scholar
  3. Ballini E, Morel JB, Droc G, Price A, Courtois B, Notteghem JL, Tharreau D (2008) A genome wde meta-analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol Plant Microbe Interact 21(7):859–868CrossRefPubMedGoogle Scholar
  4. Barry CS, Giovannoni JJ (2007) Ethylene and fruit ripening. J Plant Growth Regul 26:143–159CrossRefGoogle Scholar
  5. Bink MCAM, Jansen J, Madduri M, Voorrips RE, Durel CE, Kouassi AB, Laurens F, Mathis F, Gessler C, Gobbin D, Rezzonico F, Patocchi A, Kellerhals M, Boudichevskaia A, Dunemann F, Peil A, Nowicka A, Lata B, Stankiewicz-Kosyl M, Jeziorek K, Pitera E, Soska A, Tomala K, Evans KM, Fernández-Fernández F, Guerra W, Korbin M, Keller S, Lewandowski M, Plocharski W, Rutkowski K, Zurawicz E, Costa F, Sansavini S, Tartarini S, Komjanc M, Mott D, Antofie A, Lateur M, Rondia A, Gianfranceschi L, van de Weg WE (2014) Bayesian QTL analyses using pedigreed families of an outcrossing species, with application to fruit firmness in apple. Theor Appl Genet. doi: 10.1007/s00122-014-2281-3 PubMedGoogle Scholar
  6. Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18CrossRefPubMedGoogle Scholar
  7. Bourne MC (2002) Food texture and viscosity: concept and measurement, 2nd edn. Academic Press, San DiegoGoogle Scholar
  8. Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg WE, Parisi L, Durel E-C (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 94:370–379CrossRefPubMedGoogle Scholar
  9. Cappellin L, Farneti B, Di Guardo M, Busatto N, Khomenko I, Romano A, Velasco R, Costa G, Biasioli F, Costa F (2014) QTL analysis coupled with PTR-ToF-MS and candidate gene based association mapping validate the role of Md-AAT1 as a major gene in the control of flavor in apple. Plant Mol Biol Rep. doi: 10.1007/s11105-014-0744-y Google Scholar
  10. Chagné D, Carlisle CM, Blond C, Volz RK, Whitworth CJ et al (2007) Mapping a candidate gene (MdMYB10)for red flesh and foliage colour in apple. BMC Genomics 8:212CrossRefPubMedCentralPubMedGoogle Scholar
  11. Chagné D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C et al (2014) The draft genome sequencing of European pear (Pyrus communis L. ‘Bartlett’). Plos ONE 9(4):e92644CrossRefPubMedCentralPubMedGoogle Scholar
  12. Chagné D, Krieger C, Rassam M, Sullivan M, Fraser J, André C, Pindo M, Troggio M, Gardiner SE, Henry RA, Allan AC, McGhie TK, Laing WA (2012) QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol 12:12CrossRefPubMedCentralPubMedGoogle Scholar
  13. Chagné D, Lin-Wang K, Espley RV, Volz RK, How NM et al (2013) An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol 161:225–239CrossRefPubMedCentralPubMedGoogle Scholar
  14. Chang Y, Sun R, Sun H, Zhao Y, Han Y, Chen D, Wang Y, Zhang X, Han Z (2014) Mapping of quantitative trait loci corroborates independent genetic control of apple size and shape. Sci Hortic 174:126–132CrossRefGoogle Scholar
  15. Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196CrossRefGoogle Scholar
  16. Costa F, Cappellin L, Farneti B, Tadiello A, Romano A, Soukoulis C, Sansavini S, Velasco R, Biasioli F (2014) Advances in QTL mapping for ethylene production in apple (Malus x domestica Borkh.). Postharvest Biol Technol 87:126–132CrossRefGoogle Scholar
  17. Costa F, Cappellin L, Longhi S, Guerra W, Magnago P, Porro D, Soukoulis C, Salvi S, Velasco R, Biasioli F, Gasperi F (2011) Assessment of apple (Malus 9 domestica Borkh.) fruit texture by a combined acoustic-mechanical profiling strategy. Postharvest Biol Technol 61:21–28CrossRefGoogle Scholar
  18. Costa F, Cappellin L, Fontanari M, Longhi S, Guerra W, Magnago P, Gasperi F, Biasioli F (2012) Texture dynamics during postharvest cold storage ripening in apple (Malus × domestica Borkh.). Postharvest Biol Technol 69:54–63. doi: 10.1016/j.postharv bio.2012.03.003 CrossRefGoogle Scholar
  19. Costa F, Peace CP, Stella S, Serra S, Musacchi S, Bazzani M, Sansavini S, Van de Weg WE (2010) QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus 9 domestica Borkh.). J Exp Bot 11:2029–3039Google Scholar
  20. 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 141:181–190CrossRefGoogle Scholar
  21. Danan S, Veyrieras JB, Lefebre V (2011) Construction of a potato consensus map and QTL meta-analysis offer new insight into the genetic architecture of late blight resistance and plant maturity traits. BMC Plant Biol 11:16CrossRefPubMedCentralPubMedGoogle Scholar
  22. Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, Ling TJ, Ross JJ, Hallett IC, Gunaseelan K, Dayatilake GA, Diak R, Breen KC, Tustin DS, Costes E, Chagné D, Schaffer RJ, David KM (2012) A genomic approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12:7CrossRefPubMedCentralPubMedGoogle Scholar
  23. Dunemann F, Ulrich D, Malysheva-Otto L, Weber WE, Longhi S, Velasco R, Costa F (2012) Functional allelic diversity of the apple alcohol acyl-transferase gene MdAAT1 associated with fruit ester volatile contents in apple cultivars. Mol Breeding 29:609–625CrossRefGoogle Scholar
  24. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S et al (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427CrossRefPubMedCentralPubMedGoogle Scholar
  25. Gardner KM, Brown P, Cooke TF, Cann S, Costa F, Bustamante C, Velasco R, Troggio M, Myles S (2014) Fast and cost-effective genetic mapping in apple using next-generation sequencing. G3 (Bethesda). doi: 10.1534/g3.114.011023
  26. Gianfranceschi L, Soglio V (2004) The European project HiDRAS: innovative multidisciplinary approaches to breeding high quality disease resistant apples. Acta Horticult 663:327–330Google Scholar
  27. Giovannoni JJ (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–49CrossRefPubMedGoogle Scholar
  28. Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155(1):463–473PubMedCentralPubMedGoogle Scholar
  29. Guillon F, Philippe S, Bouchet B, Devaux MF, Frasse P, Jones B, Bouzayen M, Lahaye M (2008) Down-regulation of an auxin response factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 59(2):273–288CrossRefPubMedGoogle Scholar
  30. Guitton B, Kelner J-J, Velasco R, Gardiner SE, Chagné D, Costes E (2012) Genetic control of biennial bearing in apple. J Exp Bot 63(1):131–149CrossRefPubMedCentralPubMedGoogle Scholar
  31. Guo B, Sleper DA, Lu P, Shannon JG, Nguyen HT, Arelli PR (2006) QTLs associated with resistance to soybean cyst nematode in soybean: meta-analysis of QTL locations. Crop Sci 46(2):595–602CrossRefGoogle Scholar
  32. Hanocq E, Laperche A, Jaminon O, Laine AL, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114(3):569–584CrossRefPubMedGoogle Scholar
  33. Hao Z, Li X, Liu X, Xie C, Li M, Zhang D, Zhang S (2010) Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize. Euphytica 174:165–177CrossRefGoogle Scholar
  34. 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
  35. Holland JB (2007) Genetic architecture of complex trait in plants. Curr Opin Plant Biol 10:156–61CrossRefPubMedGoogle Scholar
  36. Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135:205–211PubMedCentralPubMedGoogle Scholar
  37. Jonkers H (1979) Biennial bearing in apple and pear: a literature survey. Sci Hortic 11:303–307CrossRefGoogle Scholar
  38. Kellerhals M, Furrer B (1994) Approaches for breeding apples with durable disease resistance. Euphytica 77:31–35CrossRefGoogle Scholar
  39. Kenis K, Keulemans J, Davey MW (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genome 4:647–661CrossRefGoogle Scholar
  40. Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breed 17:299–306CrossRefGoogle Scholar
  41. King GJ, Maliepaard C, Lynn JR, Alston FH, Durel CE, 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 100:1074–1084CrossRefGoogle Scholar
  42. Kouassi AB, Durel CE, 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, Lau- rens 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(4):659–672. doi: 10.1007/s11295-009-0217-x CrossRefGoogle Scholar
  43. Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C et al (2012) Genomic selection for fruit quality traits in apple (Malus x domestica Borkh.). Plos ONE 7(5):1–10Google Scholar
  44. Kumar S, Garrick DJ, Bink MCAM, Whitworth C, Chagné D, Volz RK (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics 14:393CrossRefPubMedCentralPubMedGoogle Scholar
  45. Kumar S, Volz RK, Chagné D, Gardiner S (2014) Breeding for apple (Malus × domestica Borkh.) fruit quality traits in the genomics era. Genomics of Plant Genetic Resources pp 387–416.Google Scholar
  46. Lacape JM, Llewellyn D, Jacobs J, Arioli T, Becker D, Calhoun S, Al-Ghazi Y, Liu SM, Palai O, Georges S (2010) Meta-analysis of cotton fiber quality QTLs across diverse environments in a Gossypium hirsutum x G. barbadense RIL population. BMC Plant Biology 10:132CrossRefPubMedCentralPubMedGoogle Scholar
  47. Lanaud C, Fouet O, Clement D, Boccara M, Risterucci AM, Surujdeo-Maharaj S, Legavre T, Argout X (2009) A meta-QTL analysis of disease resistance traits of Theobroma cacao L. Mol Breed 24(4):361–374CrossRefGoogle Scholar
  48. Li JZ, Zhang ZW, Li YL, Wang QL, Zhou YG (2011) QTL consistency and meta-analysis for grain yield components in three generation in maize. Theor Appl Genet 122:771–782CrossRefPubMedGoogle Scholar
  49. Liebhard R, Kellerhals M, Jertmini M, Gessler C (2003a) Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 52:511–526CrossRefPubMedGoogle Scholar
  50. Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003b) Cre- ating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508PubMedGoogle Scholar
  51. Longhi S, Cappellin L, Guerra W, Costa F (2013a) Validation of a functional molecular marker suitable for marker-assisted breeding for fruit texture in apple (Malus 3 domestica Borkh.). Mol Breeding 32:841–852CrossRefGoogle Scholar
  52. Longhi S, Hamblin MT, Trainotti L, Peace CP, Velasco R, Costa F (2013b) A candidate gene based approach validates Md-PG1 as the main responsible for a QTL impacting fruit texture in apple (Malus 9 domestica Borkh.). BMC Plant Biol 13:37CrossRefPubMedCentralPubMedGoogle Scholar
  53. Longhi S, Moretto M, Viola R, Velasco R, Costa F (2012) Comprehensive QTL mapping survey dissects the complex fruit texture physiology in apple (Malus × domestica Borkh.). J Exp Bot 63:1107–1121CrossRefPubMedGoogle Scholar
  54. 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 97:60–73CrossRefGoogle Scholar
  55. Maliepaard C, Sillanpaa MJ, van Ooijen JW, Jansen RC, Arjas E (2001) Bayesian versus frequentist analysis of multiple quantitative trait loci with an application to an outbred apple cross. Theor Appl Genet 103:1243–1253CrossRefGoogle Scholar
  56. Marandel G, Salava J, Abbott A, Candresse T, Decroocq V (2009) Quantitative trait loci meta-analysis of Plum pox virus resistance in apricot (Prunus armeniaca L.): new insights on the organization and the identification of genomic resistance factors. Mol Plant Pathol 10(3):347–360CrossRefPubMedGoogle Scholar
  57. Monselise S, Goldschmidt E (1982) Alternate bearing in fruit trees. Hortic Rev 4:128–173Google Scholar
  58. Paterson AH (1998) Molecular dissection of complex traits. CRC, Boca Raton, FLGoogle Scholar
  59. Patocchi A, Fernandez-Fernandez F, Evans K, Gobbin D, Re- zzonico F, Boudichevskaia A, Dunemann F, Stankiewicz- Kosyl M, Mathis-Jeanneteau F, Durel CE, Gianfranceschi L, Costa F, Toller C, Cova V, Mott D, Komjanc M, Barbaro E, Kodde L, Rikkerink E, Gessler C, van de Weg WE (2009) Development and test of 21 multiplex PCRs com- posed of SSRs spanning most of the apple genome. Tree Genet Genomes 5:211–223CrossRefGoogle Scholar
  60. Pindo M, Vezzulli S, Coppola G, Cartwright DA, Zharkikh A, Velasco R, Troggio M (2008) SNP high-throughput screening in grapevine using the SNPlexTM genotyping system. BMC Plant Biol 8:12CrossRefPubMedCentralPubMedGoogle Scholar
  61. Quraishi UM, Murat F, Abrouk M, Pont C, Confolent C, Oury FX, Ward J, Boros D, Gebruers K, Delcour JA et al (2011) Combined meta-genomics analyses unravel candidate genes for the grain dietary fiber content in bread wheat (Triticum aestivum L.). Funct Integr Genom 11:71–83CrossRefGoogle Scholar
  62. Sansavini S, Donati F, Costa F, Tartarini T (2004) Advances in apple breeding for enhanced fruit quality and resistance to biotic tresses: new varieties for the European market. J Fruit Ornamental Plant Res 12:13–51Google Scholar
  63. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–U151CrossRefPubMedCentralPubMedGoogle Scholar
  64. Sosnowski O, Charcosset A, Joets J (2012) BioMercator V3: an upgrade of genetic map compilation and QTL meta-analysis algorithms. Bioinformatics 28:2082–2083CrossRefPubMedCentralPubMedGoogle Scholar
  65. Swamy BPM, Vikram P, Dixit S, Ahmed HU, Kumar A (2011) Meta-analysis of grain yield QTL identified during agricultural drought in grasses showed consensus. BMC Genomics 12:16CrossRefGoogle Scholar
  66. Telias A, Lin-Wang K, Stevenson DE, Cooney JM, Hellens RP, Allan AC, Hoover EE, Bradeen JM (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11:93CrossRefPubMedCentralPubMedGoogle Scholar
  67. Truntzler M, BarriAre Y, Sawkins MC, Lespinasse D, Betran J, Charcosset A, Moreau L (2010) Meta-analysis of QTL involved in silage quality of maize and comparison with the position of candidate genes. Theor Appl Genet 121:1465–1482CrossRefPubMedGoogle Scholar
  68. Van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma, B.V., Wageningen, NetherlandsGoogle Scholar
  69. Van Ooijen JW (2009) MAPQTL® 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma, B.V., Wageningen, NetherlandsGoogle Scholar
  70. Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10:621–630CrossRefPubMedGoogle Scholar
  71. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839CrossRefPubMedGoogle Scholar
  72. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494CrossRefPubMedGoogle Scholar
  73. Veyrieras JB, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinforma 8:49CrossRefGoogle Scholar
  74. Visser T (1964) Juvenile phase and growth of apple and pear seedlings. Euphytica 13:119–129Google Scholar
  75. Voorrips RE (2001) MapChart version 2.0: Windows software for the graphical presentation of linkage maps and QTLs. Plant Research International, Wageningen, The NetherlandsGoogle Scholar
  76. Voorrips RE, Bink MCAM, van de Weg WE (2012) Pedimap: software for the visualization of genetic and phenotypic data in pedigrees. J Hered 103(6):903–907CrossRefPubMedCentralPubMedGoogle Scholar
  77. Xiang K, Reid LM, Zhang Z, Zhu X, Pan G (2012) Characterization of correlation between grain moisture and ear rot resistance in maize by QTL meta-analysis. Euphytica 183:185–195CrossRefGoogle Scholar
  78. Xiang K, Zhang ZM, Reid LM, Zhu XY, Yuan GS, Pan GT (2010) A meta-analysis of QTL associated with ear rot resistance in maize. Maydica 55:281–290Google Scholar
  79. Yamagishi N, Kishigami R, Yoshikawa N (2014) Reduced generation time of apple seedlings to within a year by means of a plant virus vector: a new plant-breeding technique with no transmission of genetic modification to the next generation. Plant Biotechnol J 12:60–68CrossRefPubMedGoogle Scholar
  80. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189CrossRefGoogle Scholar
  81. Young ND (1999) A cautiously optimistic vision for marker-assisted breeding. Mol Breed 5:505–510CrossRefGoogle Scholar
  82. 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 Genome 4:555–562Google Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Research and Innovation CentreFondazione Edmund MachSan Michele all’AdigeItaly

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