Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits

Plant Physiology

Volumn 165, Issue 3, 2014, Pages 1120-1132

  Sauvage, Christopher ^a   Segura, Vincent ^b   Bauchet, Guillaume ^a,c   Stevens, Rebecca ^a   Do, Phuc Thi ^d,e   Nikoloski, Zoran ^d   Fernie, Alisdair R ^d   Causse, Mathilde ^a  

^a Researches Center of Avignon   (France)

^b National Institute for Agricultural Research   (France)

^c Syngenta Seeds SAS   (France)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^e VIETNAM NATIONAL UNIVERSITY   (Viet Nam)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903589651     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.241521     Document Type: Article

References (69)

1. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655-1664
2. Astle W, Balding DJ (2009) Population structure and cryptic relatedness in genetic association studies. Stat Sci 24: 451-471
3. Aulchenko YS, Ripke S, Isaacs A, van Duijn CM(2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23: 1294-1296
4. Bauchet G, Causse M (2012) Genetic diversity in tomato (Solanum lycopersicum) and its wild relatives. In C Mahmut, ed, Genetic Diversity in Plants. InTech http://www.intechopen.com/books/genetic-diversityin-plants/genetic-diversity-in-tomato-solanum-lycopersicum-and-itswild-relatives (March 23, 2013)
5. Beleggia R, Platani C, Nigro F, De Vita P, Cattivelli L, Papa R (2013) Effect of genotype, environment and genotype-by-environment interaction on metabolite profiling in durum wheat (Triticum durum Desf.) grain. J Cereal Sci 57: 183-192
6. Bergelson J, Roux F (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11: 867-879
7. Blanca J, Cañizares J, Cordero L, Pascual L, Diez MJ, Nuez F (2012) Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS ONE 7: e48198
8. 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
9. Centeno DC, Osorio S, Nunes-Nesi A, Bertolo AL, Carneiro RT, Araújo WL, Steinhauser MC, Michalska J, Rohrmann J, Geigenberger P, et al (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23: 162-184
10. Chakrabarti M, Zhang N, Sauvage C, Muños S, Blanca J, Cañizares J, Diez MJ, Schneider R, Mazourek M, McClead J, et al (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci USA 110: 17125-17130
11. Chan EKF, Rowe HC, Kliebenstein DJ (2010) Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics 185: 991-1007
12. Chen J, Chen Z (2008) Extended Bayesian information criteria for model selection with large model spaces. Biometrika 95: 759-771
13. Etienne A, Génard M, Lobit P, Mbeguié-A-Mbéguié D, Bugaud C (2013) What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J Exp Bot 64: 1451-1469
14. 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
15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587
16. Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289: 85-88
17. Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305: 1786-1789
18. Friendly M (2002) Corrgrams: exploratory displays for correlation matrices. Am Stat 56: 316-324
19. Fulton TM, Bucheli P, Voirol E, Lopez J, Petiard V, Tanksley SD (2002) Quantitative trait loci (QTL) affecting sugars, organic acids and other biochemical properties possibly contributing to flavor, identified in four advanced backcross populations of tomato. Euphytica 127: 163-177
20. Gilbert KJ, Andrew RL, Bock DG, Franklin MT, Kane NC, Moore JS, Moyers BT, Renaut S, Rennison DJ, Veen T, et al (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program STRUCTURE. Mol Ecol 21: 4925-4930
21. Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52: 725-749
22. Gomez L, Bancel D, Rubio E, Vercambre G (2007) The microplate reader: an efficient tool for the separate enzymatic analysis of sugars in plant tissues. Validation of a micro-method. J Sci Food Agric 87: 1893-1905
23. Hamblin MT, Buckler ES, Jannink JL (2011) Population genetics of genomics-based crop improvement methods. Trends Genet 27: 98-106
24. Hamilton JP, Sim SC, Stoffel K, Van Deynze A, Buell CR, Francis DM (2012) Single nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis. Plant Genome 5: 17-29
25. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2: 612-620
26. Howie B, Fuchsberger C, Stephens M, Marchini J, Abecasis GR (2012) Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat Genet 44: 955-959
27. Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, et al (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42: 961-967
28. 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
29. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Stitt M, et al (2005) GMD@CSB. DB: the Golm Metabolome Database. Bioinformatics 21: 1635-1638
30. Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9: 29
31. Kumar S, Skjaeveland A, Orr RJ, Enger P, Ruden T, Mevik BH, Burki F, Botnen A, Shalchian-Tabrizi K (2009) AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 10: 357
32. Listgarten J, Lippert C, Kadie CM, Davidson RI, Eskin E, Heckerman D (2012) Improved linear mixed models for genome-wide association studies. Nat Methods 9: 525-526
33. Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T, et al (2010) Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci USA 107: 19585-19590
34. Mandel JR, Nambeesan S, Bowers JE, Marek LF, Ebert D, Rieseberg LH, Knapp SJ, Burke JM (2013) Association mapping and the genomic consequences of selection in sunflower. PLoS Genet 9: e1003378
35. Mangin B, Siberchicot A, Nicolas S, Doligez A, This P, Cierco-Ayrolles C (2012) Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity (Edinb) 108: 285-291
36. Marchini J, Howie B (2010) Genotype imputation for genome-wide association studies. Nat Rev Genet 11: 499-511
37. Mauricio R (2001) Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology. Nat Rev Genet 2: 370-381
38. Mounet F, Moing A, Garcia V, Petit J, Maucourt M, Deborde C, Bernillon S, Le Gall G, Colquhoun I, Defernez M, et al (2009) Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiol 149: 1505-1528
39. Muños S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier MC, Delalande C, Bouzayen M, et al (2011) Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156: 2244-2254
40. Nesbitt TC, Tanksley SD (2002) Comparative sequencing in the genus Lycopersicon: implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162: 365-379
41. Porcu E, Sanna S, Fuchsberger C, Fritsche LG (2013) Genotype imputation in genome-wide association studies. Curr Protoc Hum Genet Chapter 1: Unit 1.25
42. Powell JE, Kranis A, Floyd J, Dekkers JCM, Knott S, Haley CS (2012) Optimal use of regression models in genome-wide association studies. Anim Genet 43: 133-143
43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959
44. Prudent M, Causse M, Génard M, Tripodi P, Grandillo S, Bertin N (2009) Genetic and physiological analysis of tomato fruit weight and composition: influence of carbon availability on QTL detection. J Exp Bot 60: 923-937
45. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575
46. Ranc N, Muños S, Santoni S, Causse M (2008) A clarified position for Solanum lycopersicum var. cerasiforme in the evolutionary history of tomatoes (Solanaceae). BMC Plant Biol 8: 130
47. Ranc N, Munos S, Xu J, Le Paslier 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
48. Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci USA 109: 8872-8877
49. Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67: 175-185
50. Robbins MD, Sim SC, Yang W, Van Deynze A, van der Knaap E, Joobeur T, Francis DM (2011) Mapping and linkage disequilibrium analysis with a genome-wide collection of SNPs that detect polymorphism in cultivated tomato. J Exp Bot 62: 1831-1845
51. Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie AR (2008) Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20: 509-523
52. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24: 447-454
53. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, et al (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579: 1332-1337
54. Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q, Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44: 825-830
55. Shirasawa K, Fukuoka H, Matsunaga H, Kobayashi Y, Kobayashi I, Hirakawa H, Isobe S, Tabata S (2013) Genome-wide association studies using single nucleotide polymorphism markers developed by re-sequencing of the genomes of cultivated tomato. DNA Res 20: 593-603
56. Sillanpää MJ (2011) Overview of techniques to account for confounding due to population stratification and cryptic relatedness in genomic data association analyses. Heredity (Edinb) 106: 511-519
57. Sim SC, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S, et al (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7: e40563
58. Soto-Cerda BJ, Cloutier S (2012) Association mapping in plant genomes. In C Mahmut, ed, Genetic Diversity in Plants. InTech. http://www. intechopen.com/books/genetic-diversity-in-plants/association-mappingin-plant-genomes (April 29, 2013)
59. Steinbach D, Alaux M, Amselem J, Choisne N, Durand S, Flores RL, Keliet AO, Kimmel E, Lapalu N, Luyten I, et al (2013) GnpIS: an information system to integrate genetic and genomic data from plants and fungi. Database (Oxford) 2013: bat058
60. Stevens R, Buret M, Duffé P, Garchery C, Baldet P, Rothan C, Causse M (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 143: 1943-1953
61. Stevens R, Buret M, Garchery C, Carretero Y, Causse M (2006) Technique for rapid, small-scale analysis of vitamin C levels in fruit and application to a tomato mutant collection. J Agric Food Chem 54: 6159-6165
62. Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31: 1086-1096
63. Tabangin ME, Woo JG, Martin LJ (2009) The effect of minor allele frequency on the likelihood of obtaining false positives. BMC Proc (Suppl 7) 3: S41
64. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641
65. Visscher PM, Brown MA, McCarthy MI, Yang J (2012) Five years of GWAS discovery. Am J Hum Genet 90: 7-24
66. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370
67. Xu J, Ranc N, Muños 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
68. Zhang N, Brewer MT, van der Knaap E (2012) Fine mapping of fw3.2 controlling fruit weight in tomato. Theor Appl Genet 125: 273-284
69. Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, et al (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2: 467