Skip to main content
SpringerLink
Log in

QTL mapping of fruit nutritional and flavor components in tomato (Solanum lycopersicum) using genome-wide SSR markers and recombinant inbred lines (RILs) from an intra-specific cross

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Fruit nutritional and flavor components are important targets for breeding new cultivars of tomato (Solanum lycopersicum L.). We developed 108 recombinant inbred lines (the K39 RILs) in the F6 generation from a cross between two phenotypically different breeding lines, K03 and K09. A linkage map was constructed using 172 genome-wide simple sequence repeat markers, 3 single-nucleotide polymorphism markers, and 2 phenotypic markers. The K39 RIL map consists of 12 linkage groups (LGs) and covers a genetic distance of 1089 cM. We measured the fruit soluble solids content (SSC), titratable acidity (TA), glutamic acid content (GLU), and lycopene content (LYC) of each line in four generations (F6, F8, F10, F11), β-carotene content (CAR) in two generations, and pH in one generation. By composite interval mapping that considered yearly variations in components as non-genetic effects, we detected three quantitative trait loci (QTLs) for SSC, four for TA, two for CAR, and one each for GLU, LYC, and pH. Among them, we found two QTLs for TA in LGs 6 and 11, those for GLU and LYC were candidates for novel QTLs. QTLs detected in this study were clustered in five LGs, but we observed no apparent trade-off relationships among the QTLs in each LG. Being derived from an intra-specific cross of tomato breeding materials, these QTLs can be used in practical breeding for improving fruit quality with low risk of linkage drag.

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

Similar content being viewed by others

References

  • Aizawa K, Inakuma T (2009) Dietary capsanthin, the main carotenoid in paprika (Capsicum annuum), alters plasma high-density lipoprotein–cholesterol levels and hepatic gene expression in rats. Br J Nutr 102:1760–1766

    Article  CAS  Google Scholar 

  • Albert E, Gricourt J, Bertin N, Bonnefoi J, Pateyron S, Tamby JP, Bitton F, Causse M (2016a) Genotype by watering regime interaction in cultivated tomato: lessons from linkage mapping and gene expression. Theor Appl Genet 129:395–418

    Article  Google Scholar 

  • Albert E, Segura V, Gricourt J, Bonnefoi J, Derivot L, Causse M (2016b) Association mapping reveals the genetic architecture of tomato response to water deficit: focus on major fruit quality traits. J Exp Bot 67:6413–6430

    Article  CAS  Google Scholar 

  • Anthon GE, Barrett DM (2012) Pectin methylesterase activity and other factors affecting pH and titratable acidity in processing tomatoes. Food Chem 132:915–920

    Article  CAS  Google Scholar 

  • Ashrafi H, Kinkade MP, Merk HL, Foolad MR (2012) Identification of novel quantitative trait loci for increased lycopene content and other fruit quality traits in a tomato recombinant inbred line population. Mol Breed 30:549–567

    Article  CAS  Google Scholar 

  • Ballester AR, Molthoff J, de Vos R, Hekkert B, Orzaez D, Fernandez-Moreno JP, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol 152:71–84

    Article  CAS  Google Scholar 

  • Barrett DM, Weakley C, Diaz JV, Watnik M (2007) Qualitative and nutritional differences in processing tomatoes grown under commercial organic and conventional production systems. J Food Sci 72:C441–C451

    Article  CAS  Google Scholar 

  • Bernacchi D, Beck-Bunn T, Eshed Y, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley S (1998) Advanced backcross QTL analysis in tomato. I. Identification of QTLs for traits of agronomic importance from Lycopersicon hirsutum. Theor Appl Genet 97:381–397

    Article  CAS  Google Scholar 

  • Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York

    Book  Google Scholar 

  • Capel C, Fernandez del Carmen A, Alba JM, Lima-Silva V, Hernandez-Gras F, Salinas M, Boronat A, Angosto T, Botella MA, Fernandez-Munoz R, Granell A, Capel J, Lozano R (2015) Wide-genome QTL mapping of fruit quality traits in a tomato RIL population derived from the wild-relative species Solanum pimpinellifolium L. Theor Appl Genet 128:2019–2035

    Article  CAS  Google Scholar 

  • Capel C, Yuste-Lisbona FJ, Lopez-Casado G, Angosto T, Heredia A, Cuartero J, Fernandez-Munoz R, Lozano R, Capel J (2017) QTL mapping of fruit mineral contents provides new chances for molecular breeding of tomato nutritional traits. Theor Appl Genet 130:903–913

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chen FQ, Foolad MR, Hyman J, St. Clair DA, Beelaman RB (1999) Mapping of QTLs for lycopene and other fruit traits in a Lycopersicon esculentum × L. pimpinellifolium cross and comparison of QTLs across tomato species. Mol Breed 5:283–299

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Oliveira BF, Costa DC, Nogueira-Machado JA, Chaves MM (2013) Beta-carotene, alpha-tocopherol and ascorbic acid: differential profile of antioxidant, inflammatory status and regulation of gene expression in human mononuclear cells of diabetic donors. Diabetes Metab Res Rev 29:636–645

    Article  Google Scholar 

  • de Vicente MC, Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596

    Google Scholar 

  • Eshed Y, Zamir D (1994) Introgressions from Lycopersicon pennellii can improve the soluble-solids yield of tomato hybrids. Theor Appl Genet 88:891–897

    Article  CAS  Google Scholar 

  • Foolad MR (2007) Genome mapping and molecular breeding of tomato. Int J Plant Genom 2007:64358

    Google Scholar 

  • Frary A, Fulton TM, Zamir D, Tanksley SD (2004) Advanced backcross QTL analysis of a Lycopersicon esculentum × L. pennellii cross and identification of possible orthologs in the Solanaceae. Theor Appl Genet 108:485–496

    Article  CAS  Google Scholar 

  • Frary A, Xu Y, Liu J, Mitchell S, Tedeschi E, Tanksley S (2005) Development of a set of PCR-based anchor markers encompassing the tomato genome and evaluation of their usefulness for genetics and breeding experiments. Theor Appl Genet 111:291–312

    Article  CAS  Google Scholar 

  • Fukuoka H, Miyatake K, Negoro S, Nunome T, Ohyama A, Yamaguchi H (2008) Development of a routine procedure for single nucleotide polymorphism marker design based on the Tm-shift genotyping method. Breed Sci 58:461–464

    Article  CAS  Google Scholar 

  • Fukuoka H, Miyatake K, Nunome T, Negoro S, Shirasawa K, Isobe S, Asamizu E, Yamaguchi H, Ohyama A (2012) Development of gene-based markers and construction of an integrated linkage map in eggplant by using Solanum orthologous (SOL) gene sets. Theor Appl Genet 125:47–56

    Article  CAS  Google Scholar 

  • Fulton TM, Beck-Bunn T, Emmatty D, Eshed Y, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley SD (1997) QTL analysis of an advanced backcross of Lycopersicon peruvianum to the cultivated tomato and comparisons with QTLs found in other wild species. Theor Appl Genet 95:881–894

    Article  CAS  Google Scholar 

  • Fulton TM, Grandillo S, Beck-Bunn T, Fridman E, Frampton A, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley SD (2000) Advanced backcross QTL analysis of a Lycopersicon esculentum × Lycopersicon parviflorum cross. Theor Appl Genet 100:1025–1042

    Article  CAS  Google Scholar 

  • Fulton TM, Bucheli P, Voirol E, López J, Pétiard 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

    Article  CAS  Google Scholar 

  • Goldman IL, Paran I, Zamir D (1995) Quantitative trait locus analysis of a recombinant inbred line population derived from a Lycopersicon esculentum × Lycopersicon cheesmanii cross. Theor Appl Genet 90:925–932

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Green GY, Pereira da Costa JH, Cambiaso V, Pratta GR, Zorzoli R, Rodríguez GR (2016) Single and joint effect of the basal region of chromosome 2 and centromeric region of chromosome 8 on morphological and fruit quality traits in tomato. Euphytica 210:327–339

    Article  CAS  Google Scholar 

  • Gur A, Semel Y, Osorio S, Friedmann M, Seekh S, Ghareeb B, Mohammad A, Pleban T, Gera G, Fernie AR, Zamir D (2011) Yield quantitative trait loci from wild tomato are predominately expressed by the shoot. Theor Appl Genet 122:405–420

    Article  Google Scholar 

  • Haggard JE, Johnson EB, St Clair DA (2013) Linkage relationships among multiple QTL for horticultural traits and late blight (P. infestans) resistance on chromosome 5 introgressed from wild tomato Solanum habrochaites. G3 (Bethesda) 3:2131–2146

    Article  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    Article  CAS  Google Scholar 

  • Iwata H, Ninomiya S (2006) AntMap: constructing genetic linkage maps using an ant colony optimization algorithm. Breed Sci 56:371–377

    Article  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    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, 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

    Article  CAS  Google Scholar 

  • Nakaya A, Ichihara H, Asamizu E, Shirasawa S, Nakamura Y, Tabata S, Hirakawa H (2017) Plant genome database japan (PGDBj). Methods Mol Biol 1533:45–77

    Article  CAS  Google Scholar 

  • Ohyama A, Asamizu E, Negoro S, Miyatake K, Yamaguchi H, Tabata S, Fukuoka H (2009) Characterization of tomato SSR markers developed using BAC-end and cDNA sequences from genome databases. Mol Breed 23:685–691

    Article  CAS  Google Scholar 

  • Ohyama A, Shirasawa K, Matsunaga H, Negoro S, Miyatake K, Yamaguchi H, Nunome T, Iwata H, Fukuoka H, Hayashi T (2017) Bayesian QTL mapping using genome-wide SSR markers and segregating population derived from a cross of two commercial F1 hybrids of tomato. Theor Appl Genet 130:1601–1616

    Article  Google Scholar 

  • Pascual L, Desplat N, Huang BE, Desgroux A, Bruguier L, Bouchet JP, Le QH, Chauchard B, Verschave P, Causse M (2015) 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 13:565–577

    Article  CAS  Google Scholar 

  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pillen K, Pineda O, Candice BL, Tanksley SD (1996) Status of genome mapping tools in the taxon Solanaceae. In: Paterson AH (ed) Genome mapping in plants. R G Landes Company, Austin, pp 281–308

    Google Scholar 

  • Powell AL, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernandez-Munoz R, Vicente A, Lopez-Baltazar J, Barry CS, Liu Y, Chetelat R, Granell A, Van Deynze A, Giovannoni JJ, Bennett AB (2012) Uniform ripening encodes a golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336:1711–1715

    Article  CAS  Google Scholar 

  • Prudent M, Causse M, Genard 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

    Article  CAS  Google Scholar 

  • 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 (Bethesda) 2:853–864

    Article  CAS  Google Scholar 

  • Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sabatini E, Beretta M, Sala T, Acciarri N, Milc J, Pecchioni N (2013) Molecular breeding. In: Liedl BE, Labate JA, Stommel JR, Slade A, Kole C (eds) Genetics, genomics and breeding of tomato. Science Publishers, Enfield, pp 228–303

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sauvage C, Segura V, Bauchet G, Stevens R, Do PT, 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

    Article  CAS  Google Scholar 

  • Scott JW, James RM, Peter SB, Courtland GN, Frederic FA (2013) Classical genetics and traditional breeding. In: Liedl BE, Labate JA, Stommel JR, Slade A, Kole C (eds) Genetics, genomics and breeding of tomato. Science Publishers, Enfield, pp 37–73

    Chapter  Google Scholar 

  • Shirasawa K, Asamizu E, Fukuoka H, Ohyama A, Sato S, Nakamura Y, Tabata S, Sasamoto S, Wada T, Kishida Y, Tsuruoka H, Fujishiro T, Yamada M, Isobe S (2010a) An interspecific linkage map of SSR and intronic polymorphism markers in tomato. Theor Appl Genet 121:731–739

    Article  CAS  Google Scholar 

  • Shirasawa K, Isobe S, Hirakawa H, Asamizu E, Fukuoka H, Just D, Rothan C, Sasamoto S, Fujishiro T, Kishida Y, Kohara M, Tsuruoka H, Wada T, Nakamura Y, Sato S, Tabata S (2010b) SNP discovery and linkage map construction in cultivated tomato. DNA Res 17:381–391

    Article  CAS  Google Scholar 

  • Sim SC, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, 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:e40563

    Article  CAS  Google Scholar 

  • Sorrequieta A, Ferraro G, Boggio SB, Valle EM (2010) Free amino acid production during tomato fruit ripening: a focus on l-glutamate. Amino Acids 38:1523–1532

    Article  CAS  Google Scholar 

  • Stahl W, Sies H (2005) Bioactivity and protective effects of natural carotenoids. Biochim Biophys Acta 1740:101–107

    Article  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Röder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, Lopez J, Beck-Bunn T (1996) Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet 92:213–224

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhao J, Xu Y, Liang J, Chang P, Yan F, Li M, Liang Y, Zou Z (2015) Genome-wide association mapping for tomato volatiles positively contributing to tomato flavor. Front Plant Sci 6:1042

    PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhao J, Liang Y, Zou Z (2016) Genome-wide association-mapping for fruit quality traits in tomato. Euphytica 207:439–451

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics for Agricultural Innovation, DD4020; Development of DNA Markers for Horticultural Crop Breeding, SGE1002; Genomics-based Technology for Agricultural Improvement, NGB2005).

Author information

Author notes

  1. Hiroyuki Fukuoka

    Present address: Takii & Co., Ltd., 1360 Hari, Konan, Shiga, 520-3231, Japan

  2. Junji Kimbara and Akio Ohyama have contributed equally to this work.

Authors and Affiliations

  1. Research and Development Division, Kagome Co., Ltd., 17 Nishitomiyama, Nasushiobara-shi, Tochigi, 329-2762, Japan

    Junji Kimbara, Hiroshi Chikano, Hirotaka Ito & Katsutoshi Hosoi

  2. National Agriculture and Food Research Organization (NARO), Institute of Vegetable and Floriculture Science (NIVFS), 3-1-1 Kannondai, Tsukuba, Ibaraki, 305-8519, Japan

    Akio Ohyama

  3. NIVFS, 360 Kusawa, Ano, Tsu, Mie, 514-2392, Japan

    Satomi Negoro, Koji Miyatake, Hirotaka Yamaguchi & Tsukasa Nunome

  4. NARO Institute of Vegetable and Tea Science (NIVTS), 360 Kusawa, Ano, Tsu, Mie, 514-2392, Japan

    Hiroyuki Fukuoka

  5. NARO Institute of Crop Science (NICS), 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8518, Japan

    Takeshi Hayashi

Authors
  1. Junji Kimbara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akio Ohyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroshi Chikano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hirotaka Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsutoshi Hosoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Satomi Negoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Koji Miyatake
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hirotaka Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tsukasa Nunome
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hiroyuki Fukuoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Takeshi Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AO, JK, HC, HI, KH, TH, and HF conceived the project and designed the experiments. JK, HC and AO supervised phenotypic analysis. AO, SN, KM, HY, and TN contributed plant materials and performed DNA extraction and genotyping. AO and TH performed statistical analyses. AO, JK, and TH wrote the manuscript. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Akio Ohyama.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1008 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kimbara, J., Ohyama, A., Chikano, H. et al. QTL mapping of fruit nutritional and flavor components in tomato (Solanum lycopersicum) using genome-wide SSR markers and recombinant inbred lines (RILs) from an intra-specific cross. Euphytica 214, 210 (2018). https://doi.org/10.1007/s10681-018-2295-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-018-2295-z

Keywords

Search

Navigation