Efficiency of genomic selection for tomato fruit quality

Molecular Breeding

Volumn 36, Issue 3, 2016, Pages

  Duangjit, Janejira ^a   Causse, Mathilde ^b   Sauvage, Christopher ^b  

^a KASETSART UNIVERSITY   (Thailand)

^b Researches Center of Avignon   (France)

Author keywords

Cross validation; Fruit quality; Genomic selection; Metabolomics; SNP; Tomato

Indexed keywords

FORECASTING; FRUITS; GENES;

CROSS VALIDATION; FRUIT QUALITY; GENOMIC SELECTION; GENOMICS; METABOLOMICS; PHENOTYPIC TRAITS; PREDICTION ACCURACY; SINGLE NUCLEOTIDE POLYMORPHISMS; TOMATO; TOMATO FRUITS;

GENOME;

EID: 84960115163     PISSN: 13803743     EISSN: 15729788     Source Type: Journal    
DOI: 10.1007/s11032-016-0453-3     Document Type: Article

References (81)

1. Aflitos S, Schijlen E, de Jong H, de Ridder D, Smit S, Finkers R, Wang J, Zhang G, Li N, Mao L, Bakker F, Dirks R, Breit T, Gravendeel B, Huits H, Struss D, Swanson-Wagner R, van Leeuwen H, van Ham R, Fito L, Guignier L, Sevilla M, Ellul P, Ganko E, Kapur A, Reclus E, de Geus B, van de Geest H, Te Lintel Hekkert B, van Haarst J, Smits L, Koops A, Sanchez-Perez G, van Heusden A, Visser R, Quan Z, Min J, Liao L, Wang X, Wang G, Yue Z, Yang X, Xu N, Schranz E, Smets E, Vos R, Rauwerda J, Ursem R, Schuit C, Kerns M, vanden Berg J, Vriezen W, Janssen A, Datema E, Jahrman T, Moquet F, Bonnet J, Peters S (2014) Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J 80:136–148
2. Asoro FG, Newell MA, Beavis WD, Scott MP, Jannink JL (2011) Accuracy and training population design for genomic selection on quantitative traits in elite North American oats. Plant Genome 4:132–144
3. Bauchet G, Munos S, Sauvage C, Bonnet J, Grivet L, Causse M (2014) Genes involved in floral meristem in tomato exhibit drastically reduced genetic diversity and signature of selection. BMC Plant Biol 14:279. doi:10.1186/s12870-014-0279-2
4. Beaulieu J, Doerksen T, Clément S, MacKay J, Bousquet J (2014) Accuracy of genomic selection models in a large population of open-pollinated families in white spruce. Heredity 113:343–352
5. Beyene Y, Semagn K, Mugo S, Tarekegne A, Babu B, Meisel B, Sehabiague P, Makumbi D, Magorokosho C, Oikeh S, Gakunga J, Vargas M, Olsen M, Prasanna B, Marianne Crossa J (2015) Genetic gains in grain yield through genomic selection in eight bi-parental maize populations under drought stress. Crop Sci 55:154–163
6. Blanc G, Charcosset A, Veyrieras JB, Gallais A, Moreau L (2008) Marker-assisted selection efficiency in multiple connected populations: a simulation study based on the results of a QTL detection experiment in maize. Euphytica 161:71–84
7. Blanca J, Cañizares J, Cordero L, Pascual L, Diez M, Nuez F (2012) Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS One 7:e48198. doi:10.1371/journal.pone.0048198
8. Blanca J, Montero-Pau J, Sauvage C, Bauchet G, Illa E, Díez MJ, Francis D, Causse M, van der Knaap E, Cañizares J (2015) Genomic variation in tomato, from wild ancestors to contemporary breeding accessions. BMC Genomics 16:257. doi:10.1186/s12864-015-1444-1
9. Calus M, De Roos A, Veerkamp R (2008) Accuracy of genomic selection using different methods to define haplotypes. Genetics 178:553–561
10. Causse M, Saliba-Colombani V, Lecomte L, Duffé 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
11. Causse M, Duffe P, Gomez MC, Buret M, Damidaux R, Zamir D, Gur A, Chevalier C, Lemaire-Chamley M, Rothan C (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot 55:1671–1685
12. CoGePedia (2015) https://genomevolution.org/wiki/index.php/Sequenced_plant_genomes
13. Cros D, Denis M, Sánchez L, Cochard B, Flori A, Durand-Gasselin T, Nouy B, Omoré A, Pomiès V, Riou V, Suryana E, Bouvet JM (2014) Genomic selection prediction accuracy in a perennial crop: case study of oil palm (Elaeis guineensis Jacq.). Theor Appl Genet 128:397–410
14. Crossa J, Beyene Y, Kassa S, Perez P, Hickey JM, Chen C, de los Campos G, Burgueno J, Windhausen VS, Buckler E, Jannink JL, Lopez Cruz MA, Babu R (2013) Genomic prediction in maize breeding populations with genotyping-by-sequencing. G3 G3(3):1903–1926
15. Daetwyler HD, Calus MPL, Pong-Wong R, de los Campos G, Hickey JM (2013) Genomic prediction in animals and plants: simulation of data, validation, reporting, and benchmarking. Genetics 193:347–365
16. El-Dien OG, Ratcliffe B, Klapste J, Chen C, Porth I, El-KAssaby Y (2015) Prediction accuracies for growth and wood attributes of interior spruce in space using genotyping-by-sequencing. BMC Genomics 1–16(13):370
17. Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255
18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
19. Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
20. Frary A, Nesbitt T, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert K, Tanksley S (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
21. Fridman E, Pleban T, Zamir D (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97:4718–4723
22. Gianola D, Okut H, Weigel K, Rosa G (2011) Predicting complex quantitative traits with Bayesian neural networks: a case study with Jersey cows and wheat. BMC Genet 12:87. doi:10.1186/1471-2156-12-87
23. González-Camacho J, de los Campos G, Pérez P, Gianola D, Cairns J, Mahuku G, Raman B, Crossa J (2012) Genome-enabled prediction of genetic values using radial basis function neural networks. Theor Appl Genet 125:759–771
24. Gouy M, Rousselle Y, Bastianelli D, Lecomte P, Bonnal L, Roques D, Efile JC, Rocher S, Daugrois L, Toubi L, Nabeneza S, Hervouet C, Telismart H, Denis M, Thong-Chane A, Glaszmann JC, Hoarau JY, Nibouche S, Costet L (2013) Experimental assessment of the accuracy of genomic selection in sugarcane. Theor Appl Genet 126:2575–2586
25. Habier D, Fernando RL, Dekkers JCM (2007) The impact of genetic relationship information on genome-assisted breeding values. Genetics 177:2389–2397
26. Habier D, Tetens J, Seefried F, Lichtner P, Thaller G (2010) The impact of genetic relationship information on genomic breeding values in German Holstein cattle. Genet Sel Evol 42:5. doi:10.1186/1297-9686-42-5
27. Hamilton J, Buell C (2012) Advances in plant genome sequencing. Plant J 70:177–190
28. Hayes B, Bowman P, Chamberlain A, Goddard M (2009) Genomic selection in dairy cattle: progress and challenges. J Dairy Sci 92:433–443
29. Heffner EL, Sorrells ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12
30. Heslot N, Yang HP, Sorrells ME, Jannink JL (2012) Genomic selection in plant breeding: a comparison of models. Crop Sci 52:146–160
31. Hickey JM, Gorjanc G (2012) Simulated data for genomic selection and genome-wide association studies using a combination of coalescent and gene drop methods. G3 2:425–427. doi:10.1534/g3.111.001297/-/DC1
32. Hirakawa H, Shirasawa K, Miyatake K, Nunome T, Negoro S, Ohyama A, Yamaguchi H, Sato S, Isobe S, Tabata S, Fukuoka H (2014) Draft genome sequence of eggplant (Solanum melongena L.): the representative Solanum species indigenous to the old world. DNA Res 21(6):649–660
33. Howard R, Carriquiry AL, Beavis WD (2014) Parametric and nonparametric statistical methods for genomic selection of traits with additive and epistatic genetic architectures. G3 4:1027–1046
34. Isidro J, Jannink J, Akdemir D, Poland J, Heslot N, Sorrells M (2015) Training set optimization under population structure in genomic selection. Theor Appl Genet 128:145–158
35. Jonas E, de Koning D-J (2013) Does genomic selection have a future in plant breeding? Trends Biotechnol 31:497–504
36. Jones D, Thomas C, Hammondkosack K, Balintkurti P, Jones J (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793
37. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723
38. Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C, Carlisle C (2012) Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.). PLoS One 7:e36674. doi:10.1371/journal.pone.0036674
39. Lecomte L, Duffé P, Buret M, Servin B, Hospital F, Causse M (2004) Marker-assisted introgression of 5 QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. Theor Appl Genet 109:658–668
40. Lin T, Zhu G, Zhang J, Xu X, Yu Q, Zheng Z, Zhang Z, Lun Y, Li S, Wang X, Huang Z, Li J, Zhang C, Wang T, Zhang Y, Wang A, Zhang Y, Lin K, Li C, Xiong G, Xue Y, Mazzucato A, Causse M, Fei Z, Giovannoni JJ, Chetelat RT, Zamir D, Stadler T, Li J, Ye Z, Du Y, Huang S (2014) Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46:1220–1226
41. Lorenz A, Smith K, Jannink J (2012) Potential and optimization of genomic selection for Fusarium head blight resistance in six-row barley. Crop Sci 52:1609–1621
42. Maltecca C, Kristen ParkerKL, Cassady JP (2012) Application of multiple shrinkage methods to genomic predictions. J Anim Sci 90:1777–1787
43. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TFC, McCarroll SA, Visscher PM (2009) Finding the missing heritability of complex diseases. Nature 461:747–753
44. Martin G, Brommonschenkel S, Chunwongse J, Frary A, Ganal M, Spivey R, Wu T, Earle E, Tanksley S (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436
45. Meuwissen T (2007) Genomic selection: marker assisted selection on a genome wide scale. J Anim Breed Genet 124:321–322
46. Meuwissen T, Hayes B, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
47. Meuwissen T, Hayes B, Goddard M (2013) Accelerating improvement of livestock with genomic selection. Annu Rev Anim Biosci 1:221–237
48. Michael T, VanBuren R (2015) Progress, challenges and the future of crop genomes. Curr Opin Plant Biol 24:71–81
49. Muños S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier M, Delalande C, Bouzayen M, Brunel D, Causse M (2011) Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156:2244–2254
50. Owens B, Lipka A, Magallanes-Lundback M, Tiede T, Diepenbrock C, Kandianis C, Kim E, Cepela J, Mateos-Hernandez M, Buell C, Buckler E, DellaPenna D, Gore M, Rocheford T (2014) A foundation for provitamin a biofortification of maize: genome-wide association and genomic prediction models of carotenoid levels. Genetics 198:1699–1716
51. Pascual L, Desplat N, Huang BE, Desgroux A, Bruguier L, Bouchet J-P, Le QH, Chauchard B, Verschave P, Causse M (2014) Potential of a tomato MAGIC population to decipher the genetic control of quantitative traits and detect causal variants in the resequencing era. Plant Biotechnol J. doi:10.1111/pbi.12282
52. Pascual L, Albert E, Sauvage C, Duangjit J, Bouchet J, Bitton F, Desplat N, Brunel D, Paslier M, Ranc N, Bruguier L, Chauchard B, Verschave P, Causse M (2016) Dissecting quantitative trait variation in the resequencing era: complementarity of bi-parental, multi-parental and association panels. Plant Sci 242:120–130
53. Pérez P, de los Campos G (2014) Genome-wide regression and prediction with the BGLR statistical package. Genetics 198(2):483–495
54. Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216
55. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M, Bender D, Maller J, Sklar P, de Bakker P, Daly M, Sham P (2007) PLINK: a toolset for whole-genome association and population-based linkage analysis. Am J Hum Genet 81:559–575
56. Qin C et al (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111:5135–5140
57. Ranc N, Munos S, Xu J, LePaslier MC, Chauveau A, Bounon R, Rolland S, Bouchet JP, Brunel D, Causse M (2012) Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3 2:853–864
58. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN: 3-900051-07-0, http://www.R-project.org
59. Resende JM, Muñoz P, Resende M, Garrick D, Fernando R, Davis J, Jokela E, Martin T, Peter G, Kirst M (2012) Accuracy of genomic selection methods in a standard data set of Loblolly Pine (Pinus taeda L.). Genetics 190:1503–1510
60. Rincent R, Laloë D, Nicolas S, Altmann T, Brunel D, Revilla P, Rodríguez V, Moreno-Gonzalez J, Melchinger A, Bauer E, Schoen C, Meyer N, Giauffret C, Bauland C, Jamin P, Laborde J, Monod H, Flament P, Charcosset A, Moreau L (2012) Maximizing the reliability of genomic selection by optimizing the calibration set of reference individuals: comparison of methods in two diverse groups of maize inbreds (Zea mays L.). Genetics 192:715–728
61. Ruggieri V, Francese G, Sacco A, D’Alessandro A, Rigano MM, Parisi M, Milone M, Cardi T, Mennella G, Barone A (2014) An association mapping approach to identify favourable alleles for tomato fruit quality breeding. BMC Plant Biol 14:337. doi:10.1186/s12870-014-0337-9
62. Sacco A, Ruggieri V, Parisi M, Festa G, Rigano MM, Picarella ME, Mazzucato A, Barone A (2015) Exploring a tomato landraces collection for fruit-related traits by the aid of a high-throughput genomic platform. PLoS One. doi:10.1371/journal.pone.0137139
63. Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, Kaneko T, Nakamura Y, Shibata D, Aoki K, Egholm M, Knight J, Bogden R, Li C, Shuang Y, Xu X, Pan S, Cheng S, Liu X, Ren Y, Wang J, Albiero A, Dal Pero F, Todesco S, Van Eck J, Buels RM, Bombarely A, Gosselin JR, Huang M, Leto JA, Menda N, Strickler S, Mao L, Gao S, Tecle IY, York T, Zheng Y, Vrebalov JT, Lee J, Zhong S, Mueller LA, Stiekema WJ, Ribeca P, Alioto T, Yang W, Huang S, Du Y, Zhang Z, Gao J, Guo Y, Wang X, Li Y, He J, Li C, Cheng Z, Zuo J, Ren J, Zhao J, Yan L, Jiang H, Wang B, Li H, Li Z, Fu F, Chen B, Han B, Feng Q, Fan D, Wang Y, Ling H, Xue Y, Ware D, McCombie WR, Lippman ZB, Chia JM, Jiang K, Pasternak S, Gelley L, Kramer M, Anderson LK, Chang SB, Royer SM, Shearer LA, Stack SM, Rose JKC, Xu Y, Eannetta N, Matas AJ, McQuinn R, Tanksley SD, Camara F, Guigo R, Rombauts S, Fawcett J, Van de Peer Y, Zamir D, Liang C, Spannagl M, Gundlach H, Bruggmann R et al (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
64. Sauvage C, Segura V, Bauchet G, Stevens R, Phuc Thi D, Nikoloski Z, Fernie AR, Causse M (2014) Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol 165:1120–1132
65. Sim SC, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S, Francis DM (2012a) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One 7:e40563. doi:10.1371/journal.pone.0040563
66. Sim SC, Van DeynzeA, Stoffel K, Douches DS, Zarka D, Ganal MW, Chetelat RT, Hutton SF, Scott JW, Gardner RG, Panthee DR, Mutschler M, Myers JR, Francis DM (2012b) High-density SNP genotyping of tomato (Solanum lycopersicum L.) reveals patterns of genetic variation due to breeding. PLoS One 7:e45520. doi:10.1371/journal.pone.0045520
67. Solberg TR, Sonesson AK, Woolliams JA, Meuwissen TH (2008) Genomic selection using different marker types and densities. J Anim Sci 86:2447–2454
68. Spindel J, Begum H, Akdemir D, Virk P, Collard B, Redona E, Atlin G, Jannink JL, McCouch S (2015) Genomic selection and association mapping in rice (Oryza sativa): effect of trait genetic architecture, training population composition, marker number and statistical model on accuracy of rice genomic selection in elite, tropical rice breeding lines. PLoS Genet 11:e1004982
69. Storlie E, Charmet G (2013) Genomic selection accuracy using historical data generated in a wheat breeding program. Plant Genome. doi:10.3835/plantgenome2013.01.0001
70. Tanksley SD, Fulton TM (2007) Dissecting quantitative trait variation-examples from the tomato. Euphytica 154:365–370
71. Tanksley S, Ganal M, Prince J, de-Vicente M, Bonierbale M, Broun P, Fulton T, Giovannoni J, Grandillo S, Martin G, Messeguer R, Miller J, Miller L, Paterson A, Pineda O, Roder M, Wing R, Wu W, Young N (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160
72. Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley S (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172:2529–2540
73. Wang Y, Mette M, Miedaner T, Gottwald M, Wilde P, Reif J, Zhao Y (2014) The accuracy of prediction of genomic selection in elite hybrid rye populations surpasses the accuracy of marker-assisted selection and is equally augmented by multiple field evaluation locations and test years. BMC Genomics 15:556. doi:10.1186/1471-2164-15-556
74. Wimmer V, Lehermeier C, Albrecht T, Auinger H, Wang Y, Schön C (2013) Genome-wide prediction of traits with different genetic architecture through efficient variable selection. Genetics 195:573–587
75. Windhausen VS, Atlin GN, Hickey JM, Crossa J, Jannink JL, Sorrells ME, Raman B, Cairns JE, Tarekegne A, Semagn K, Beyene Y, Grudloyma P, Technow F, Riedelsheimer C, Melchinger AE (2012) Effectiveness of genomic prediction of maize hybrid performance in different breeding populations and environments. G3 2:1427–1436. doi:10.1534/g3.112.003699
76. Würschum T, Reif J, Kraft T, Janssen G, Zhao Y (2013) Genomic selection in sugar beet breeding populations. BMC Genet 14:1–8. doi:10.1186/1471-2156-14-85
77. Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De la Cruz G, Chakrabarti SK, Patil VU, Skryabin KG, Kuznetsov BB, Ravin NV, Kolganova TV, Beletsky AV, Mardanov AV, Di Genova A, Bolser DM, Martin DMA, Li G, Yang Y, Kuang H, Hu Q, Xiong X, Bishop GJ, Sagredo B, Mejia N, Zagorski W, Gromadka R, Gawor J, Szczesny P, Huang S, Zhang Z, Liang C, He J, Li Y, He Y, Xu J, Zhang Y, Xie B, Du Y, Qu D, Bonierbale M, Ghislain M, del Rosario HerreraM, Giuliano G, Pietrella M, Perrotta G, Facella P, O’Brien K, Feingold SE, Barreiro LE, Massa GA, Diambra L, Whitty BR, Vaillancourt B, Lin H, Massa A, Geoffroy M, Lundback S, DellaPenna D, Buell CR, Sharma SK, Marshall DF, Waugh R, Bryan GJ, Destefanis M, Nagy I, Milbourne D, Thomson SJ, Fiers M, Jacobs JME, Nielsen KL, Sonderkaer M, Iovene M, Torres GA, Jiang J, Veilleux RE, Bachem CWB, de Boer J, Borm T, Kloosterman B, van Eck H, Datema E, Hekkert BTL, Goverse A, van Ham RCHJ, Visser RGF, Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. doi:10.1038/nature10158
78. Xu Y, Lu Y, Xie C, Gao S, Wan J, Prasanna B (2012) Whole-genome strategies for marker-assisted plant breeding. Mol Breed 29:833–854
79. Xu J, Ranc N, Munos S, Rolland S, Bouchet JP, Desplat N, Le Paslier MC, Liang Y, Brunel D, Causse M (2013) Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor Appl Genet 126:567–581
80. Zhang X, Pérez-Rodríguez P, Semagn K, Beyene Y, Babu R, López-Cruz M, Vicente F, Olsen M, Buckler E, Jannink J, Prasanna B, Crossa J (2015) Genomic prediction in biparental tropical maize populations in water-stressed and well-watered environments using low-density and GBS SNPs. Heredity 114:291–299
81. Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20