Skip to main content
SpringerLink
Log in

Use of modern tomato breeding germplasm for deciphering the genetic control of agronomical traits by Genome Wide Association study

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A panel of 300 tomato accessions including breeding materials was built and characterized with >11,000 SNP. A population structure in six subgroups was identified. Strong heterogeneity in linkage disequilibrium and recombination landscape among groups and chromosomes was shown. GWAS identified several associations for fruit weight, earliness and plant growth.

Abstract

Genome-wide association studies (GWAS) have become a method of choice in quantitative trait dissection. First limited to highly polymorphic and outcrossing species, it is now applied in horticultural crops, notably in tomato. Until now GWAS in tomato has been performed on panels of heirloom and wild accessions. Using modern breeding materials would be of direct interest for breeding purpose. To implement GWAS on a large panel of 300 tomato accessions including 168 breeding lines, this study assessed the genetic diversity and linkage disequilibrium decay and revealed the population structure and performed GWA experiment. Genetic diversity and population structure analyses were based on molecular markers (>11,000 SNP) covering the whole genome. Six genetic subgroups were revealed and associated to traits of agronomical interest, such as fruit weight and disease resistance. Estimates of linkage disequilibrium highlighted the heterogeneity of its decay among genetic subgroups. Haplotype definition allowed a fine characterization of the groups and their recombination landscape revealing the patterns of admixture along the genome. Selection footprints showed results in congruence with introgressions. Taken together, all these elements refined our knowledge of the genetic material included in this panel and allowed the identification of several associations for fruit weight, plant growth and earliness, deciphering the genetic architecture of these complex traits and identifying several new loci useful for tomato breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbo S, Pinhasi van-Oss R, Gopher A, Saranga Y, Ofner I, Peleg Z (2014) Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci 19:351–360

    Article  CAS  PubMed  Google Scholar 

  • Aflitos S, Schijlen E, de Jong H, de Ridder D, Smit S, Finkers R, Wang J, Zhang G, Li N, Mao L et al (2014) Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J 80:136–148

    Article  PubMed  Google Scholar 

  • Akey JM, Zhang K, Xiong M, Jin L (2003) The effect of single nucleotide polymorphism identification strategies on estimates of linkage disequilibrium. Mol Biol Evol 20(2):232–242

    Article  CAS  PubMed  Google Scholar 

  • Albrechtsen A, Nielsen FC, Nielsen R (2010) Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 27(11):2534–2547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alseekh S, Ofner I, Pleban T, Tripodi P, Di Dato F, Cammareri M, Mohammad A, Grandillo S, Fernie AR, Zamir D (2013) Resolution by recombination: breaking up Solanum pennellii introgressions. Trends Plant Sci 18:536–538

    Article  CAS  PubMed  Google Scholar 

  • Arnold B, Corbett-Detig RB, Hartl D, Bomblies K (2013) RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Mol Ecol 22(11):3179–3190

    Article  CAS  PubMed  Google Scholar 

  • Astle W, Balding DJ (2009) Population structure and cryptic relatedness in genetic association studies. Stat Sci 24(4):451–471

    Article  Google Scholar 

  • Barb JG, Bowers JE, Renaut S, Rey JI, Knapp SJ, Rieseberg LH, Burke JM (2014) Chromosomal evolution and patterns of introgression in Helianthus. Genetics 197(3):969–979

    Article  PubMed  PubMed Central  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. ICWSM 8:362

    Google Scholar 

  • Bates DM, Watts DG (2008) Nonlinear regression analysis and its applications. Wiley, Hoboken

    Google Scholar 

  • Bauchet G, Causse M (2012) Genetic diversity in tomato (Solanum lycopersicum) and its wild relatives. In: Genetic diversity in plants. PMC: InTech

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bi K, Vanderpool D, Singhal S, Linderoth T, Moritz C, Good J (2012) Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genom 13(1):403

    Article  CAS  Google Scholar 

  • Blanca J, Montero-Pau J, Sauvage C, Bauchet G, Illa E, Diez MJ, Francis D, Causse M, van der Knaap E, Cañizares J (2015) Genomic variation in the tomato, from wild ancestors to contemporary breeding accessions. BMC Genom 16:257. doi:10.1186/s12864-015-1444-1

    Article  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genet 172(2):1165–1177

    Article  Google Scholar 

  • Cao Y, Tang X, Giovannoni J, Xiao F, Liu Y (2012) Functional characterization of a tomato COBRA-like gene functioning in fruit development and ripening. BMC Plant Biol 12:211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casals J, Pascual L, Cañizares J, Cebolla-Cornejo J, Casañas F, Nuez F (2011) The risks of success in quality vegetable markets: possible genetic erosion in Marmande tomatoes (Solanum lycopersicum L.) and consumer dissatisfaction. Sci Hortic 130(1):78–84

    Article  Google Scholar 

  • Causse M, Friguet C, Coiret C, Lépicier M, Navez B, Lee M, Holthuysen N, Sinesio F, Moneta E, Grandillo S (2010) Consumer preferences for fresh tomato at the European scale: a common segmentation on taste and firmness. J Food Sci 75(9):S531–S541

    Article  CAS  PubMed  Google Scholar 

  • Causse M, Desplat N, Pascual L, Le Paslier M-C, Sauvage C, Bauchet G, Berard A, Bounon R, Tchoumakov M, Brunel D, Bouchet JP (2013) Whole genome resequencing in tomato reveals variation associated with introgression and breeding events. BMC Genom 14(1):791

    Article  CAS  Google Scholar 

  • Chakrabarti M, Zhang N, Sauvage C, Munos S, Blanca J, Canizares J, Diez MJ, Schneider R, Mazurek M, McClead J, Causse M, van der Knaap E (2013) A cytochrome P450 CYP78A regulates a domestication trait in tomato (Solanum lycopersicum). Proc Natl Acad Sci USA PNAS 110(42):17125–17130

    Article  CAS  PubMed  Google Scholar 

  • Chen A-L, Liu C-Y, Chen C-H, Wang J-F, Liao Y-C, Chang C-H, Tsai M-H, Hwu K-K, Chen K-Y (2014) Reassessment of QTLs for late blight resistance in the tomato accession L3708 using a restriction site associated DNA (RAD) linkage map and highly aggressive isolates of Phytophthora infestans. PLoS One 9(5):e96417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Consortium TGP (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491(7422):56–65

    Article  CAS  Google Scholar 

  • Corrado G, Piffanelli P, Caramante M, Coppola M, Rao R (2013) SNP genotyping reveals genetic diversity between cultivated landraces and contemporary varieties of tomato. BMC Genom 14(1):835

    Article  Google Scholar 

  • Desta ZA, Ortiz R (2014) Genomic selection: genome-wide prediction in plant improvement. Trends Plant Sci 19(9):592–601

    Article  CAS  PubMed  Google Scholar 

  • Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding Leucine-Rich repeat proteins. Cell 84:451–459

    Article  CAS  PubMed  Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127(7):1309–1321

    Article  CAS  PubMed  Google Scholar 

  • Duangjit J, Causse M, Sauvage C (2016) Efficiency of genomic selection for tomato fruit quality. Mol Breed. doi:10.1007/s11032-016-0453-3

    Google Scholar 

  • Ersoz E, Yu J, Buckler E (2007) Applications of linkage disequilibrium and association mapping in crop plants. In: Varshney R, Tuberosa R (eds) Genomics-assisted crop improvement. Springer, Netherlands, p 97–119

    Chapter  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9(10):e1003905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–87

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Pozo N, Menda M, Edwards JD, Saha S, Tecle IY, Strickler SR, Bombarely A, Fisher-York T, Pujar A, Foerster H, Yan A, Mueller LA (2014) The Sol Genomics Network (SGN)—from genotype to phenotype to breeding. Nucl Acids Res. doi:10.1093/nar/gku1195 (first published online 26 Nov 2014)

    PubMed  PubMed Central  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180(2):977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraïsse C, Roux C, Welch JJ, Bierne N (2014) Gene-flow in a mosaic hybrid zone: is local introgression adaptive? Genetics 197(3):939–951

    Article  PubMed  PubMed Central  Google Scholar 

  • Frary A, Nesbitt TC, Frary A, Grandillo S, Van Der Knaap E, Cong B et al (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289(5476):85–88

    Article  CAS  PubMed  Google Scholar 

  • Fridman E, Zamir D (2012) Next-generation education in crop genetics. Curr Opin Plant Biol 15(2):218–223

    Article  PubMed  Google Scholar 

  • Gautier M, Vitalis R (2013) Inferring population histories using genome-wide allele frequency data. Mol Biol Evol 30(3):654–668

    Article  CAS  PubMed  Google Scholar 

  • Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156(1–2):1–13

    Article  Google Scholar 

  • Hamilton JP, Sim S-C, Stoffel K, Van Deynze A, Buell CR, Francis DM (2012) Single nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis. Plant Gen 5(1):17–29

    Article  CAS  Google Scholar 

  • Harlan JR (1971) Agricultural origins: centers and noncenters. Science 174(4008):468–474

    Article  CAS  PubMed  Google Scholar 

  • Hellenthal G, Busby GBJ, Band G, Wilson JF, Capelli C, Falush D, Myers S (2014) A genetic atlas of human admixture history. Science 343(6172):747–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    Article  CAS  PubMed  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33(1):54–78

    Article  CAS  PubMed  Google Scholar 

  • Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J (2013) The genomic signature of crop-wild introgression in maize. PLoS Genet 9(5):e1003477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang K, Liberatore KL, Park SJ, Alvarez JP, Lippman ZB (2013) Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet 9(12):e1004043

    Article  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11(1):94

    Article  PubMed  PubMed Central  Google Scholar 

  • Jonas E, de Koning DJ (2013) Does genomic selection have a future in plant breeding?. Trends Biotechnol 31: 497–504

    Article  CAS  Google Scholar 

  • Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P et al (1998) Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol Gen Genet MGG 257(3):376–385

    Article  CAS  PubMed  Google Scholar 

  • 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(3):1709–1723

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ et al (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci 98(11):6511–6515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koenig D, Jiménez-Gómez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV, Tohge T, Bolger A, Schneeberger K, Ossowski S, Lanz C, Xiong G, Taylor-Teeples M, Brady SM, Pauly M, Weigel D, Usadel B, Fernie AR, Peng J, Sinha NR, Maloof JN (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci 110:2655–2662

    Article  CAS  Google Scholar 

  • Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9(1):29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korte A, Vilhjalmsson BJ, Segura V, Platt A, Long Q, Nordborg M (2012) A mixed-model approach for genome-wide association studies of correlated traits in structured populations. Nat Genet 44(9):1066–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labate J, Robertson L (2012) Evidence of cryptic introgression in tomato (Solanum lycopersicum L.) based on wild tomato species alleles. BMC Plant Biol 12(1):133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labate J, Grandillo S, Fulton T, Muños S, Caicedo A, Peralta I, Ji Y, Chetelat R, Scott JW, Gonzalo MJ, Francis D, Yang W, van der Knaap E, Baldo AM, Smith-White B, Mueller LA, Prince JP, Blanchard NE, Storey DB, Stevens MR, Robbins MD, Fen Wang J, Liedl BE, O’Connell MA, Stommel JR, Aoki K, Iijima Y, Slade, Hurst SR, Loeffler D, Steine MN, Vafeados D, McGuire C, Freeman C, Amen A, Goodstal J, Facciotti D, Van Eck J, Causse M (2007) 1 Tomato. In: Kole C (ed) Genome mapping and molecular breeding in plants, volume 5, vegetables. Springer-Verlag, Berlin, p 11–135

    Google Scholar 

  • Labate JA, Robertson LD, Strickler SR, Mueller LA (2014) Genetic structure of the four wild tomato species in the Solanum peruvianum s.l. species complex. Genome 57(3):169–180

    Article  CAS  PubMed  Google Scholar 

  • Lachance J, Tishkoff SA (2013) SNP ascertainment bias in population genetic analyses: why it is important, and how to correct it. Bioessays 35(9):780–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanfermeijer F, Dijkhuis J, Sturre MG, de Haan P, Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Mol Biol 52(5):1039–1051

    Article  Google Scholar 

  • Lawson DJ, Falush D (2012) Population identification using genetic data. Annu Rev Genom Hum Genet 13(1):337–361

    Article  CAS  Google Scholar 

  • Lawson DJ, Hellenthal G, Myers S, Falush D (2012) Inference of population structure using dense haplotype data. PLoS Genet 8(1):e1002453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Stephens M (2003) Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165(4):2213–2233

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin T, Zhu G, Zhang J, Xu X, Yu Q, Zheng Z, Zhang Z, Lun Y, Li S, Wang X et al (2014) Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46:1220–1226

    Article  CAS  PubMed  Google Scholar 

  • 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(5138):1432–1436

    Article  CAS  PubMed  Google Scholar 

  • McCouch S, Baute GJ, Bradeen J, Bramel P, Bretting PK, Buckler E, Burke JM, Charest D, Cloutier S, Cole G et al (2013) Agriculture: feeding the future. Nature 499(7456):23–24

    Article  CAS  PubMed  Google Scholar 

  • McGill JR, Walkup EA, Kuhner MK (2013) Correcting coalescent analyses for panel-based SNP ascertainment. Genetics 193(4):1185–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer RS, Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14(12):840–852

    Article  CAS  PubMed  Google Scholar 

  • Michalak P, Zhao K, Wright M, Kimball J, Eizenga G, McClung A, Kovach M, Tyagi W, Ali ML, Tung C-W et al (2010) Genomic Diversity and Introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS One 5(5):e10780

    Article  CAS  Google Scholar 

  • Monforte AJ, Diaz AI, Caño-Delgado A, van der Knaap E (2014) The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. J Exp Bot 65:4625–4637

    Article  CAS  PubMed  Google Scholar 

  • Nielsen R, Signorovitch J (2003) Correcting for ascertainment biases when analyzing SNP data: applications to the estimation of linkage disequilibrium. Theor Popul Biol 63(3):245–255

    Article  PubMed  Google Scholar 

  • Pfeifer B, Wittelsbürger U, Ramos Onsins SE, Lercher MJ (2014) PopGenome: an efficient swiss army knife for population genomic analyses in R. Mol Biol Evol 31:1929–1936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens P, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, 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(3):559–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranc N, Muños 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rincent R, Moreau L, Monod H, Kuhn E, Melchinger AE, Malvar RA, Moreno-Gonzalez J, Nicolas S, Madur D, Combes V, Dumas F, Altmann T, Brunel D, Ouzunova M, Flament P, Dubreuil P, Charcosset A, Mary-Huard T (2014) Recovering power in association mapping panels with variable levels of linkage disequilibrium. Genetics 197(1):375–387

    Article  PubMed  PubMed Central  Google Scholar 

  • Sacco A, Ruggieri V, Parisi M, Festa G, Rigano MM, Picarella ME et al (2015) Exploring a tomato landraces collection for fruit-related traits by the aid of a high-throughput genomic platform. PLoS One 10(9):e0137139. doi:10.1371/journalpone.0137139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarah G, Homa F, Pointet S, Contreras S, Sabot F, Nabholz B, Santoni S, Sauné L, Ardisson M, Chantret N, Sauvage C, Tregear J, Jourda C, Pot D, Vigouroux Y, Chair H, Scarcelli N, Billot C, Yahiaoui N, Bacilieri R, Khadari B, Boccara M, Barnaud A, Péros J-P, Labouisse J-P, Pham J-L, David J, Glémin S, Ruiz M (2016) A large set of 26 new reference transcriptomes dedicated to comparative population genomics in crops and wild relatives. Mol Ecol Resour. doi:10.1111/1755-0998.12587

    PubMed  Google Scholar 

  • Sauvage C, Segura V, Bauchet G, Stevens R, Thi Do P, Nikoloski Z, Fernie AR, Causse M (2014) Genome Wide Association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol 165(3):1120–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78(4):629–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeb JE, Carvalho G, Hauser L, Naish K, Roberts S, Seeb LW (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Mol Ecol Resour 11:1–8

    Article  PubMed  Google Scholar 

  • Segura V, Vilhjalmsson BJ, Platt A, Korte A, Seren U, Long Q, Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44(7):825–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sim S-C, Van Deynze A, Stoffel K, Douches DS, Zarka D, Ganal MW, Chetelat RT, Hutton SF, Scott JW, Gardner RG et al (2012a) High-density SNP genotyping of tomato reveals patterns of genetic variation due to breeding. PLoS One 7(9):e45520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sim S-C, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S et al (2012b) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One 7(7):e40563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Speed D, Hemani G, Johnson Michael R, Balding David J (2012) Improved heritability estimation from genome-wide SNPs. Am J Hum Genet 91(6):1011–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277(5329):1063–1066

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB et al (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132(4):1141–1160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400):635–641

    Article  CAS  Google Scholar 

  • van Berloo R (2008) GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 99(2):232–236

    Article  PubMed  CAS  Google Scholar 

  • Van Deynze A, Stoffel K, Buell CR, Kozik A, Liu J, van der Knaap E, Francis D (2007) Diversity in conserved genes in tomato. BMC Genom 8(1):465

    Article  Google Scholar 

  • Varshney RK, Ribaut J-M, Buckler ES, Tuberosa R, Rafalski JA, Langridge P (2012) Can genomics boost productivity of orphan crops? Nat Biotech 30(12):1172–1176

    Article  CAS  Google Scholar 

  • Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RGF, Scott JW, Edwards JD, Bai Y (2013) The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-class RNA–dependent RNA polymerases. PLoS Genet 9(3):e1003399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viquez-Zamora M, Vosman B, van de Geest H, Bovy A, Visser R, Finkers R, van Heusden A (2013) Tomato breeding in the genomics era: insights from a SNP array. BMC Genom 14(1):354

    Article  CAS  Google Scholar 

  • Waugh R, Francki M, Marshall D, Thomas B, Comadran J, Russell J, Close T, Stein N, Hayes P, Muehlbauer G, Cockram J, O’Sullivan D, Mackay I, Flavell A, Ramsay L (2010) Whole-genome association mapping in elite inbred crop varieties. Genome 53(11):967–972

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J org Evol 38(6):1358–1370

    Article  Google Scholar 

  • Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L et al (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30(1):105–111

    Article  CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208

    Article  CAS  PubMed  Google Scholar 

  • Zamir D (2008) Plant breeders go back to nature. Nat Genet 40(3):269–270

    Article  CAS  PubMed  Google Scholar 

  • Zamir D, Ekstein-Michelson I, Zakay Y, Navot N, Zeidan M, Sarfatti M, Eshed Y, Harel E, Pleban T, van-Oss H et al (1994) Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1. Theor Appl Genet 88(2):141–146

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Liu L, Zheng Z, Sun Y, Zhou L, Yang Y, Cheng F, Zhang Z, Wang X, Huang S et al (2013) Fine mapping of the Ph-3 gene conferring resistance to late blight (Phytophthora infestans) in tomato. Theor Appl Genet 126(10):2643–2653

    Article  CAS  PubMed  Google Scholar 

  • Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28(24):3326–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome J 1(1):5

    Article  CAS  Google Scholar 

  • Zuriaga E, Blanca JM, Cordero L, Sifres A, Blas-Cerdán WG, Morales R, Nuez F (2008) Genetic and bioclimatic variation in Solanum pimpinellifolium. Genet Resour Crop Evol 56(1):39–51

    Article  Google Scholar 

Download references

Acknowledgements

We thank the CRBLeg group in INRA for providing accessions and Stephane Deville and Sandrine Paulin for genotyping. Syngenta and Association Française pour la Recherche et la Technologie (ANRT) funded this work.

Author information

Author notes

  1. Guillaume Bauchet

    Present address: Boyce Thompson Institute, Cornell University, 533 Tower Rd, Ithaca, NY, 14853, USA

Authors and Affiliations

  1. Syngenta Seeds, 12 Chemin de l’Hobit, 31790, Saint Sauveur, France

    Guillaume Bauchet, Stéphane Grenier, Nicolas Samson, Julien Bonnet & Laurent Grivet

  2. INRA, UR1052, Centre de Recherche PACA, GAFL, 67 Allée des Chênes, Domaine Saint Maurice, CS60094, 84143, Montfavet Cedex, France

    Guillaume Bauchet & Mathilde Causse

Authors
  1. Guillaume Bauchet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stéphane Grenier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Samson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julien Bonnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laurent Grivet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mathilde Causse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mathilde Causse.

Ethics declarations

Conflict of interest

Authors declared no conflict of interest in the authorship and publication of this document.

Additional information

Communicated by Hong-Qing Ling.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 50 KB)

Supplementary material 2 (PPTX 20643 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bauchet, G., Grenier, S., Samson, N. et al. Use of modern tomato breeding germplasm for deciphering the genetic control of agronomical traits by Genome Wide Association study. Theor Appl Genet 130, 875–889 (2017). https://doi.org/10.1007/s00122-017-2857-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2857-9

Keywords

Search

Navigation