Feasibility of genome-wide association analysis using a small single nucleotide polymorphism panel in an apple breeding population segregating for fruit skin color

Journal of the American Society for Horticultural Science

Volumn 139, Issue 6, 2014, Pages 619-626

  Lozano, Lidia ^a,d   Iglesias, Ignasi ^a   Micheletti, Diego ^b   Troggio, Michela ^b   Kumar, Satish ^c   Volz, Richard K ^c   Allan, Andrew C ^c   Chagné, David ^c   Gardiner, Susan E ^c  

^a IRTA   (Spain)

^b RESEARCH AND INNOVATION CENTRE   (Italy)

^c THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^d Res Ctr for Agric/Forest L   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MALUS X DOMESTICA;

EID: 84913601488     PISSN: 00031062     EISSN: 23279788     Source Type: Journal    
DOI: 10.21273/jashs.139.6.619     Document Type: Article

References (56)

1. Akhunov, E., C. Nicolet, and J. Dvorak. 2009. Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor. Appl. Genet. 119:507-517.
2. Arakawa, O. 1991. Effect of temperature on anthocyanin accumulation in apple fruit as affected by cultivar, stage of fruit ripening and bagging. J. Hort. Sci. 66:763-768.
3. Baugher, T.A., H.W.J. Hogmire, and G.W. Lightner. 1990. Determining apple packout losses and impact on profitability. Appl. Agr. Res. 5:343-349.
4. Boyer, J. and R. Liu. 2004. Apple phytochemicals and their health benefits. Nutr. J. 3:5.
5. Chagné, D., C.M. Carlisle, C. Blond, R.K. Volz, C.J. Whitworth, N.C. Oraguzie, R.N. Crowhurst, A.C. Allan, R.V. Espley, R.P. Hellens, and S.E. Gardiner. 2007. Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212.
6. Chagné, D., R.N. Crowhurst, M. Pindo, A. Thrimawithana, C. Deng, H. Ireland, M. Fiers, H. Dzierzon, A. Cestaro, P. Fontana, L. Bianco, A. Lu, R. Storey, M. Knäbel, M. Saeed, S. Montanari, Y.K. Kim, D. Nicolini, S. Larger, E. Stefani, A.C. Allan, J. Bowen, I. Harvey, J. Johnston, M. Malnoy, M. Troggio, L. Perchepied, G. Sawyer, C. Wiedow, K. Won, R. Viola, R.P Hellens, L. Brewer, V.G.M. Bus, R.J. Schaffer, S.E. Gardiner, and R. Velasco. 2014. The draft genome sequence of European pear (Pyrus communis L. ‘Bartlett’). PLoS ONE 9(4):e92644.
7. Chagné, D., R.N. Crowhurst, M. Troggio, M.W. Davey, B. Gilmore, C. Lawley, S. Vanderzande, R.P. Hellens, S. Kumar, A. Cestaro, R. Velasco, D. Main, J.D. Rees, A. Iezzoni, T. Mockler, L. Wilhelm, E. van de Weg, S.E. Gardiner, N. Bassil, C. Peace, and M. Bendahmane. 2012a. Genome-wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One 7:e31745.
8. Chagné, D., K. Lin-Wang, R.V. Espley, R.K. Volz, N.M. How, S. Rouse, C. Brendolise, C.M. Carlisle, S. Kumar, N. de Silva, D. Micheletti, T. McGhie, R.N. Crowhurst, R.D. Storey, R. Velasco, R.P. Hellens, S.E. Gardiner, and A.C. Allan. 2012b. An ancient duplication of apple MYB transcription factors is responsible for novel red fruitflesh phenotypes. Plant Physiol. 161:225-239.
9. Chagné, D., K. Gasic, R.N. Crowhurst, Y. Han, H.C. Bassett, D.R. Bowatte, T.J. Lawrence, E.H. Rikkerink, S.E. Gardiner, and S.S. Korban. 2008. Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353-358.
10. Cheng, F.S., N.F. Weeden, and S.K. Brown. 1996. Identification of codominant RAPD markers tightly linked to fruit skin color in apple. Theor. Appl. Genet. 933:222-227.
11. Collard, B.C. and D.J. Mackill. 2008. Marker-assisted selection: An approach for precision plant breeding in the twenty-first century. Phil. Trans. Royal Soc. B Biol. Sci. 363:557-572.
12. Curry, E.A. 1997. Temperatures for optimum anthocyanin accumulation in apple tissue. J. Hort. Sci. 72:723-729.
13. Dickinson, J.P. and A.G. White. 1986. Red colour distribution in the skin of Gala apple and some of its sports. N. Z. J. Agr. Res. 29:695-698.
14. Eckert, A.J., B. Pande, E.S. Ersoz, M.H. Wright, V.K. Rashbrook, C.M. Nicolet, and D.B. Neale. 2009. High-throughput genotyping and mapping of single nucleotide polymorphisms in loblolly pine (Pinus taeda L.). Tree Genet. Genomes 5:225-234.
15. Elshire, R.J., J.C. Glaubitz, Q. Sun, J.A. Poland, K. Kawamoto, E.S. Buckler, S.E. Mitchell, and L. Orban. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379.
16. Espley, R.V., R.P. Hellens, J. Putterill, D.E. Stevenson, S. Kutty-Amma, and A.C. Allan. 2007. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 49:414-427.
17. Fan, J.B., M.S. Chee, and K.L. Gunderson. 2006. Highly parallel genomic assays. Nat. Rev. Genet. 7:632-644.
18. Faragher, J.D. 1983. Temperature regulation of anthocyanin accumulation in apple skin. J. Expt. Bot. 34:1291-1298.
19. Gardiner, S.E., J.L. Norelli, N. de Silva, G. Fazio, A. Peil, M. Malnoy, M. Horner, D. Bowatte, C. Carlisle, C. Wiedow, Y. Wan, C.L. Bassett, A.M. Baldo, J.M. Celton, K. Richter, H.S. Aldwinckle, and V.G.M. Bus. 2012. Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus ‘Robusta 5’ accessions. BMC Genet. 13:25.
20. Gaut, B.S. 2003. The lowdown on linkage disequilibrium. Plant Cell 15:1502-1506.
21. Hyten, D.L., Q. Song, I.Y. Choi, M.S. Yoon, J.E. Specht, L.K. Matukumalli, R.L. Nelson, R.C. Shoemaker, N.D. Young, and P.B. Cregan. 2008. High-throughput genotyping with the GoldenGate assay in the complex genome of soybean. Theor. Appl. Genet. 116:945-952.
22. Iglesias, I. and S. Alegre. 2006. The effect of anti-hail nets on fruit protection, radiation, temperature, quality and profitability of ‘Mondial Gala’ apples. J. Appl. Hort. 8:91-100.
23. Iglesias, I., G. Echeverría, and Y. Soria. 2008. Differences in fruit colour development, anthocyanin content, fruit quality and consumer acceptability of eight ‘Gala’ apple strains. Sci. Hort. 119:32-40.
24. Khan, M.A., C.E. Durel, B. Duffy, D. Drouet, M. Kellerhals, C. Gessler, and A. Patocchi. 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 50:568-577.
25. Khan, M.A., Y. Han, Y.F. Zhao, and S.S. Korban. 2012. A highthroughput apple SNP genotyping platform using the GoldenGate_assay. Gene 494:196-201.
26. Kumar, S., M.C.A.M. Bink, R.K. Volz, V.G.M. Bus, and D. Chagné. 2012. Towards genomic selection in apple (Malus domestica Borkh.) breeding programmes: Prospects, challenges and strategies. Tree Genet. Genomes 8:1-14.
27. Kumar, S., D.J. Garrick, M.C. Bink, C. Whitworth, D. Chagné, and R.K. Volz. 2013. Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics 14:393.
28. Lancaster, J. and D.K. Dougall. 1992. Regulation of skin color in apples. Crit. Rev. Plant Sci. 10:487-502.
29. Laurens, F., M.J. Aranzana, P. Arus, J. Bonany, L. Corelli, B. Diep, A. Patocchi, A. Peil, B. Quilot, S. Salvi, E. Van de Weg, and A. Vecchietti. 2010. FruitBreedomics: A new European initiative to bridge the gap between scientific research and breeding Rosaceae fruit tree crops. Intl. Hort. Congr. Lisbon, Portugal. Intl. Soc. Hort. Sci., Louvain, Belgium. p. 242 (abstr.).
30. Lewis, P.O. and D. Zaykin. 2001. Genetic data analysis: Computer program for the analysis of allelic data, Version 1.0 (d16c). 15 Nov. 2012. .
31. Lin-Wang, K.U., D. Micheletti, J. Palmer, R. Volz, L. Lozano, R. Espley, R.P. Hellens, D. Chagnè, D.D. Rowan, M. Troggio, I. Iglesias, and A.C. Allan. 2011. High temperature reduces apple fruit colour viamodulation of the anthocyanin regulatory complex. Plant Cell Environ. 34:1176-1190.
32. Lipka, A.E., F. Tian, Q. Wang, J. Peiffer, M. Li, P.J. Bradbury, M.A. Gore, E.S. Buckler, and Z. Zhang. 2012. GAPIT: Genome association and prediction integrated tool. Bioinformatics 28:2397-2399.
33. Maliepaard, C., F.H. Alston, G. van Arkel, L.M. Brown, E. Chevreau, F. Dunemann, K.M. Evans, S. Gardiner, P. Guilford, A.W. van Heusden, J. Janse, F. Laurens, J.R. Lynn, A.G. Manganaris, A.P.M. den Nijs, N. Periam, E. Rikkerink, P. Roche, C. Ryder, S. Sansavini, H. Schmidt, S. Tartarini, J.J. Verhaegh, M. Vrielink-van Ginkel, and G.J. King. 1998. Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor. Appl. Genet. 97:60-73.
34. Martinez-Garcia, P.J., J. Fresnedo-Ramirez, D.E. Parfitt, T.M. Gradziel, and C.H. Crisosto. 2013. Effect prediction of identified SNPs linked to fruit quality and chilling injury in peach [Prunus persica (L.) Batsch]. Plant Mol. Biol. 81:161-174.
35. McGhie, T.K., M. Hunt, and L.E. Barnett. 2005. Cultivar and growing region determine the antioxidant polyphenolic concentration and composition of apples grown in New Zealand. J. Agr. Food Chem. 53:3065-3070.
36. McGuire, R.G. 1992. Reporting of objective color measurements. HortScience 27:1254-1255.
37. Micheletti, D., M. Troggio, A. Zharkikh, F. Costa, M. Malnoy, R. Velasco, and S. Salvi. 2011. Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genet. Genomes 7:857-868.
38. Myles, S., J. Peiffer, P.J. Brown, E.S. Ersoz, Z. Zhang, D.E. Costich, and E.S. Buckler. 2009. Association mapping: Critical considerations shift from genotyping to experimental design. Plant Cell 21:2194-2202.
39. Patocchi, A., M. Walser, S. Tartarini, G.A.L. Broggini, F. Gennari, S. Sansavini, and C. Gessler. 2005. Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630-636.
40. Rafalski, A. 2002. Applications of single nucleotide polymorphisms in crop genetics. Curr. Opin. Plant Biol. 5:94-100.
41. Rostoks, N., L. Ramsay, K. MacKenzie, L. Cardle, P.R. Bhat, M.L. Roose, J.T. Svensson, N. Stein, R.K. Varshney, D.F. Marshall, A. Graner, T.J. Close, and R. Waugh. 2006. Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc. Natl. Acad. Sci. USA 103:18656-18661.
42. Saure, M.C. 1990. External control of anthocyanin formation in apple. Sci. Hort. 42:181-218.
43. Shulaev, V., D.J. Sargent, R.N. Crowhurst, T.C. Mockler, O. Folkerts, A.L. Delcher, P. Jaiswal, K. Mockaitis, A. Liston, S.P. Mane, P. Burns, T.M. Davis, J.P. Slovin, N. Bassil, R.P. Hellens, C. Evans, T. Harkins, C. Kodira, B. Desany, O.R. Crasta, R.V. Jensen, A.C. Allan, T.P. Michael, J.C. Setubal, J.M. Celton, D.J.G. Rees, K.P. Williams, S.H. Holt, J.J.R. Rojas, M. Chatterjee, B. Liu, H. Silva, L. Meisel, A. Adato, S.A. Filichkin, M. Troggio, R. Viola, T.L. Ashman, H. Wang, P. Dharmawardhana, J. Elser, R. Raja, H.D. Priest, D.W. Bryant, S.E. Fox, S.A. Givan, L.J. Wilhelm, S. Naithani, A. Christoffels, D.Y. Salama, J. Carter, E.L. Girona, A. Zdepski, W. Wang, R.A. Kerstetter, W. Schwab, S.S. Korban, J. Davik, A. Monfort, B. Denoyes-Rothan, P. Arus, R. Mittler, B. Flinn, A. Aharoni, J.L. Bennetzen, S.L. Salzberg, A.W. Dickerman, R. Velasco, M. Borodovsky, R.E. Veilleux, and K.M. Folta. 2011. The genome of woodland strawberry (Fragaria vesca). Nat. Genet. 43:109-116.
44. Soufflet-Freslon, V., L. Gianfranceschi, A. Patocchi, and C.E. Durel. 2008. Inheritance studies of apple scab resistance and identification of Rvi14 a new major gene that acts together with other broadspectrum QTL. Genome 51:657-667.
45. Takos, A.M., F.W. Jaffe, S.R. Jacob, J. Bogs, S.P. Robinson, and A.R. Walker. 2006. Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 142:1216-1232.
46. Ubi, B.E., C. Honda, H. Bessho, S. Kondo, M. Wada, S. Kobayashi, and T. Moriguchi. 2006. Expression analysis of anthocyanin biosynthetic genes in apple skin: Effect of UV-B and temperature. Plant Sci. 170:571-578.
47. VanRaden, P.M. 2008. Efficient methods to compute genomic predictions. J. Dairy Sci. 91:4414-4423.
48. Varshney, R.K., S.N. Nayak, G.D. May, and S.A. Jackson. 2009. Nextgeneration sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol. 27:522-530.
49. Velasco, R., A. Zharkikh, J. Affourtit, A. Dhingra, A. Cestaro, A. Kalyanaraman, P. Fontana, S.K. Bhatnagar, M. Troggio, D. Pruss, S. Salvi, M. Pindo, P. Baldi, S. Castelletti, M. Cavaiuolo, G. Coppola, F. Costa, V. Cova, A. Dal Ri, V. Goremykin, M. Komjanc, S. Longhi, P. Magnago, G. Malacarne, M. Malnoy, D. Micheletti, M. Moretto, M. Perazzolli, A. Si-Ammour, S. Vezzulli, E. Zini, G. Eldredge, L.M. Fitzgerald, N. Gutin, J. Lanchbury, T. Macalma, J.T. Mitchell, J. Reid, B. Wardell, C. Kodira, Z. Chen, B. Desany, F. Niazi, M. Palmer, T. Koepke, D. Jiwan, S. Schaeffer, V. Krishnan, C. Wu, V.T. Chu, S.T. King, J. Vick, Q. Tao, A. Mraz, A. Stormo, K. Stormo, R. Bogden, D. Ederle, A. Stella, A. Vecchietti, M.M. Kater, S. Masiero, P. Lasserre, Y. Lespinasse, A.C. Allan, V. Bus, D. Chagné, R.N. Crowhurst, A.P. Gleave, E. Lavezzo, J.A. Fawcett, S. Proost, P. Rouzé, L. Sterck, S. Toppo, B. Lazzari, R.P. Hellens, C.E. Durel, A. Gutin, R.E. Bumgarner, S.E. Gardiner, M. Skolnick, M. Egholm, Y. van de Peer, F. Salamini, and R. Viola. 2010. The genome of the domesticated apple (Malus · domestica Borkh.). Nat. Genet. 42:833-839.
50. Verde, I., A.G. Abbott, S. Scalabrin, S. Jung, S. Shu, F. Marroni, T. Zhebentyayeva, M.T. Dettori, J. Grimwood, F. Cattonaro, A. Zuccolo, L. Rossini, J. Jenkins, E. Vendramin, L.A. Meisel, V. Decroocq, B. Sosinski, S. Prochnik, T. Mitros, A. Policriti, G. Cipriani, L. Dondini, S. Ficklin, D.M. Goodstein, P. Xuan, C.D. Fabbro, V. Aramini, D. Copetti, S. Gonzalez, D.S. Horner, R. Falchi, S. Lucas, E. Mica, J. Maldonado, B. Lazzari, D. Bielenberg, R. Pirona, M. Miculan, A. Barakat, R. Testolin, A. Stella, S. Tartarini, P. Tonutti, P. Arús, A. Orellana, C. Wells, D. Main, G. Vizzotto, H. Silva, F. Salamini, J. Schmutz, M. Morgante, and D.S. Rokhsar. 2013. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat. Genet. 45:487-494.
51. Verde, I., N. Bassil, S. Scalabrin, B. Gilmore, C.T. Lawley, K. Gasic, D. Micheletti, U.R. Rosyara, F. Cattonaro, E. Vendramin, D. Main, V. Aramini, A.L. Blas, T.C. Mockler, D.W. Bryant, L. Wilhelm, M. Troggio, B. Sosinski, M.J. Aranzana, P. Arús, A. Iezzoni, M. Morgante, C. Peace, and R. Wu. 2012. Development and evaluation of a 9K SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PLoS ONE 7:e35668.
52. Weir, S.B., Sunderland, MA., Wu, J., Z. Wang, Z. Shi, S. Zhang, R. Ming, S. Zhu, M.A. Khan, S. Tao, S.S. Korban, H. Wang, N.J. Chen, T. Nishio, X. Xu, L. Cong, K. Qi, X. Huang, Y. Wang, X. Zhao, C. Deng, C. Gou, W. Zhou, H. Yin, G. Qin, Y. Sha, Y. Tao, H. Chen, Y. Yang, Y. Song, D. Zhan, J. Wang, L. Li, M. Dai, C. Gu, D. Shi, X. Wang, H. Zhang, L. Zeng, D. Zheng, C. Wang, M. Chen, G. Wang, L. Xie, V. Sovero, S. Sha, W. Huang, M. Zhang, J. Sun, L. Xu, Y. Li, X. Liu, Q. Li, J. Shen, R.E. Paull, and J.L. Bennetzen. 2013. 1996. Genetic data analysis II. Methods for discrete population genetics data. 2nd Ed. Sinauer Assoc., The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res. 23:396-408.
53. Xie, X.B., S. Li, R.F. Zhang, J. Zhao, Y.C. Chen, Q. Zhao, Y.X. Yao, C.X. You, X.S. Zhang, and Y.J. Hao. 2012. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ. 35:1884-1897.
54. Yan, J., X. Yang, T. Shah, H. Sánchez-Villeda, J. Li, M. Warburton, Y. Zhou, J.H. Crouch, and Y. Xu. 2010. High-throughput SNP genotyping with the GoldenGate assay in maize. Mol. Breed. 25:441-451.
55. Zaykin, D.V. 2004. Bounds and normalization of the composite linkage disequilibrium coefficient. Genet. Epidemiol. 27:252-257.
56. Zhu, Y., K. Evans, and C. Peace. 2011. Utility testing of an apple skin color MdMYB1 marker in two progenies. Mol. Breed. 27:525-532.