Abstract
Association mapping has been proposed as an efficient approach to assist in the identification of the molecular basis of agronomical traits in plants. For this purpose, we analyzed the phenotypic and genetic diversity of a large collection of tomato accessions including 44 heirloom and vintage cultivars (Solanum lycopersicum), 127 S. lycopersicum var. cerasiforme (cherry tomato) and 17 Solanum pimpinellifolium accessions. The accessions were genotyped using a SNPlex™ assay of 192 SNPs, among which 121 were informative for subsequent analysis. Linkage disequilibrium (LD) of pairwise loci and population structure were analyzed, and the association analysis between SNP genotypes and ten fruit quality traits was performed using a mixed linear model. High level of LD was found in the collection at the whole genome level. It was lower when considering only the 127 S. lycopersicum var. cerasiforme accessions. Genetic structure analysis showed that the population was structured into two main groups, corresponding to cultivated and wild types and many intermediates. The number of associations detected per trait varied, according to the way the structure was taken into account, with 0–41 associations detected per trait in the whole collection and a maximum of four associations in the S. lycopersicum var. cerasiforme accessions. A total of 40 associations (30 %) were co-localized with previously identified quantitative trait loci. This study thus showed the potential and limits of using association mapping in tomato populations.
Similar content being viewed by others
References
Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356
Aranzana MJ, Kim S, Zhao KY, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang CL, Toomajian C, Traw B, Zheng HG, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:531–539
Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng DZ, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JDG, Michael T, Nemri A, Roux F, Salt DE, Tang CL, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631
Barrero LS, Tanksley SD (2004) Evaluating the genetic basis of multiple-locule fruit in a broad cross section of tomato cultivars. Theor Appl Genet 109:669–679
Berard A, Le Paslier MC, Dardevet M, Exbrayat-Vinson F, Bonnin I, Cenci A, Haudry A, Brunel D, Ravel C (2009) High-throughput single nucleotide polymorphism genotyping in wheat (Triticum spp.). Plant Biotechnol J 7:364–374
Bergelson J, Roux F (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11:867–879
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Causse M, Saliba-Colombani V, Lecomte L, Duffe 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
Causse M, Buret M, Robini K, Verschave P (2003) Inheritance of nutritional and sensory quality traits in fresh market tomato and relation to consumer preferences. J Food Sci 68:2342–2350
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
Davies JN, Hobson GE (1981) The constituents of tomato fruit—the influence of environment, nutrition, and genotype. Crit Rev Food Sci Nutr 15:205–280
De La Vega FA, Lazaruk KD, Rhodes MD, Wenz MH (2005) Assessment of two flexible and compatible SNP genotyping platforms: TaqMan (R) SNP genotyping assays and the SNPlex (TM) genotyping system. Mutat Res Fundam Mol Mech Mutagen 573:111–135
Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162
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
Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Frary A, Nesbitt TC, Grandillo S, van der Knaap E, Cong B, Liu JP, 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
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
Goldman IL, Paran I, Zamir D (1995) Quantitative trait locus analysis of a recombinant inbred line population derived from a Lycopersicon esculentum x Lycopersicon cheesmanii cross. Theor Appl Genet 90:925–932
Grandillo S, Tanksley SD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92:935–951
Hall D, Tegstrom C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 9:157–165
Hamblin MT, Warburton ML, Buckler ES (2007) Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. Plos One 2(12):e1367
Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Laval G, SanCristobal M, Chevalet C (2002) Measuring genetic distances between breeds: use of some distances in various short term evolution models. Genet Select Evol 34:481–507
Lecomte L, Saliba-Colombani V, Gautier A, Gomez-Jimenez MC, Duffe P, Buret M, Causse M (2004) Fine mapping of QTLs of chromosome 2 affecting the fruit architecture and composition of tomato. Mol Breed 13:1–14
Mamidi S, Chikara S, Goos RJ, Hyten DL, Annam D, Moghaddam SM, Lee RK, Cregan PB, McClean PE (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164
Mazzucato A, Papa R, Bitocchi E, Mosconi P, Nanni L, Negri V, Picarella ME, Siligato F, Soressi GP, Tiranti B, Veronesi F (2008) Genetic diversity, structure and marker-trait associations in a collection of Italian tomato (Solanum lycopersicum L.) landraces. Theor Appl Genet 116:657–669
Mezmouk S, Dubreuil P, Bosio M, Decousset L, Charcosset A, Praud S, Mangin B (2011) Effect of population structure corrections on the results of association mapping tests in complex maize diversity panels. Theor Appl Genet 122:1149–1160
Miller JC, Tanksley SD (1990) RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor Appl Genet 80:437–448
Moonsamy PV, Bonella PL, Williams TC, Holcomb CL, Turenchalk GS, Blake LA, Hoglund BN, Rastrou M, Daigle DA, Simen BB, Goodridge D, Hillman G, Hamilton A, May AP, Erlich HA (2011) Use of the fluidigm (R) access array (TM) system provides simplified amplicon library preparation in next generation sequencing for high throughput hla genotyping. Hum Immunol 72:S142–S142
Munos S, Ranc N, Botton E, Berard A, Rolland S, Duffe P, Carretero Y, Le Paslier MC, 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
Nemri A, Atwell S, Tarone AM, Huang YS, Zhao K, Studholme DJ, Nordborg M, Jones JD (2010) Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc Natl Acad Sci USA 107:10302–10307
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
Orsini E, Krchov LM, Uphaus J, Melchinger AE (2012) Mapping of QTL for resistance to first and second generation of European corn borer using an integrated SNP and SSR linkage map. Euphytica 183:197–206
Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD (1991) Mendelian factors underlying quantitative traits in tomato—comparison across species, generations, and environments. Genetics 127:181–197
Pindo M, Vezzulli S, Coppola G, Cartwright DA, Zharkikh A, Velasco R, Troggio M (2008) SNP high-throughput screening in grapevine using the SNPlex (TM) genotyping system. BMC Plant Biol 8:128
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Ranc N, Munos 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
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. Genes Genomes Genet 2:853–864
Robbins MD, Sim SC, Yang WC, 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
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272
Sim S-C, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Robin Buell C, Causse M, Wijeratne S, Francis DM (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One 7(7):e40563. doi:10.1371/journal.pone.0040563
Szalma SJ, Hostert BM, LeDeaux JR, Stuber CW, Holland JB (2007) QTL mapping with near-isogenic lines in maize. Theor Appl Genet 114:1211–1228
Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:U113–U159
Tobler AR, Short S, Andersen MR, Paner TM, Briggs JC, Lambert SM, Wu PP, Wang Y, Spoonde AY, Koehler RT, Peyret N, Chen C, Broomer AJ, Ridzon DA, Zhou H, Hoo BS, Hayashibara KC, Leong LN, Ma CN, Rosenblum BB, Day JP, Ziegle JS, De La Vega FM, Rhodes MD, Hennessy KM, Wenz HM (2005) The SNPlex genotyping system: a flexible and scalable platform for SNP genotyping. J Biomol Tech (JBT) 16:398–406
van Berloo R, Zhu AG, Ursem R, Verbakel H, Gort G, van Eeuwijk FA (2008) Diversity and linkage disequilibrium analysis within a selected set of cultivated tomatoes. Theor Appl Genet 117:89–101
van der Knaap E, Tanksley SD (2001) Identification and characterization of a novel locus controlling early fruit development in tomato. Theor Appl Genet 103:353–358
van der Knaap E, Tanksley SD (2003) The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in Yellow Stuffer tomato. Theor Appl Genet 107:139–147
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 Genomics 8:465
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang JK, Wan XY, Crossa J, Crouch J, Weng JF, Zhai HQ, Wan JM (2006) QTL mapping of grain length in rice (Oryza sativa L.) using chromosome segment substitution lines. Genet Res 88:93–104
Yu JM, Pressoir G, Briggs WH, Bi IV, 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 38:203–208
Zhao H, Nettleton D, Soller M, Dekkers JCM (2005) Evaluation of linkage disequilibrium measures between multi-allelic markers as predictors of linkage disequilibrium between markers and QTL. Genet Res 86:77–87
Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467
Acknowledgments
The research was financed by INRA AIP Bioresources project. Jiaxin Xu was supported by China Scholarship Council. We thank Hélène Burck for characterizing and maintaining the INRA tomato Genetic Resources collection. We are grateful to Yolande Carretero, Esther Pelpoir and Laure David for their help with growing and phenotyping cherry tomato accessions.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Havey.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, J., Ranc, N., Muños, S. et al. Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor Appl Genet 126, 567–581 (2013). https://doi.org/10.1007/s00122-012-2002-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-012-2002-8