Skip to main content

Advertisement

SpringerLink
Log in

QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines

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

Abstract

Antioxidants present in fruits and vegetables may help prevent some chronic diseases such as cancer, arthritis, and heart disease. Tomatoes provide a major contribution to human dietary nutrition because of their widespread consumption in fresh and processed forms. A tomato introgression line population that combines single chromosomal segments introgressed from the wild, green fruited species Lycopersicon pennellii in the background of the domesticated tomato, Lycopersicon esculentum, was used to identify quantitative trait loci (QTL) for nutritional and antioxidant contents. The concentration of ascorbic acid, total phenolics, lycopene and β-carotene, and the total antioxidant capacity of the water-soluble fraction (TACW) were measured in the ripe fruits. A total of 20 QTL were identified, including five for TACW (ao), six for ascorbic acid (aa), and nine for total phenolics (phe). Some of these QTL (ao6-2, ao6-3, ao7-2, ao10-1, aa12-4, phe6-2, and phe7-4) increased levels as compared to the parental line L. esculentum. For lycopene content, we detected four QTL, but none increased levels relative to L. esculentum. The two QTL (bc6-2 and bc6-3) detected for β-carotene increased its levels. The traits studied displayed a strong environmental interaction as only 35% of the water-soluble antioxidant QTL (including TACW, ascorbic, and phenolic contents) were consistent over at least two seasons. Also, only two QTL for phenolics were observed when plants were grown in the greenhouse and none was detected for ascorbic or TACW. The analysis demonstrates that the introgression of wild germplasm may improve the nutritional quality of tomatoes; however regulation appears to be complex with strong environmental effects.

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

Similar content being viewed by others

References

  1. Alpert KB, Tanksley SD (1996) High-resolution mapping and isolation of a yeast artificial chromosome contig containing fw2.2: a major fruit weight quantitative trait locus in tomato. Proc Natl Acad Sci USA 93:15503–15507

    Article  PubMed  CAS  Google Scholar 

  2. Astua-Monge G, Minsavage GV, Stall RE, Vallejos CE, Davis MJ, Jones JB (2000) Xv4-vrxv4: a new gene-for-gene interaction identified between Xanthomonas campestris pv vesicatoria race T3 and the wild tomato relative Lycopersicon pennellii. Mol Plant Microbe Interact 13:1346–1355

    Article  PubMed  CAS  Google Scholar 

  3. Beggs CJ, Wellmann E (1985) Analysis of light-controlled anthocyanin formation in coleoptiles of Zea mays L: the role of UV-B, blue and far-reed light. Photochem Photobiol 41:481–486

    Article  CAS  Google Scholar 

  4. 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 

  5. Demmig-Adams B, Adams WWR (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  7. Dunnet CW (1955) A multiple comparison procedure for comparing several treatments with a single control. J Am Statist Assoc 50:1096–1121

    Article  Google Scholar 

  8. Eshed Y, Zamir D (1994a) A genomic library of Lycopersicon pennellii in L esculentum: A tool for fine mapping of genes. Euphytica 79:175–179

    Article  CAS  Google Scholar 

  9. Eshed Y, Zamir D (1994b) A genomic library of Lycopersicon pennellii in L esculentum: A tool for the fine mapping of genes. Euphytica 79:175–179

    Article  CAS  Google Scholar 

  10. 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

    PubMed  CAS  Google Scholar 

  11. Eshed Y, Abu-Abied M, Saranga Y, Zamir D (1992) Lycopersicon esculentum lines containing small overlapping introgressions from L pennellii. Theor Appl Genet 79:175–179

    Google Scholar 

  12. Eshed Y, Gera G, Zamir D (1996) A genome-wide search for wild-species alleles that increase horticultural yield of processing tomatoes. Theor Appl Genet 93:877–886

    Article  CAS  Google Scholar 

  13. Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22:589–602

    Article  PubMed  CAS  Google Scholar 

  14. Fridman E, Liu YS, Carmel-Goren L, Gur A, Shoresh M, Pleban T, Eshed Y, Zamir D (2002) Two tightly linked QTLs modify tomato sugar content via different physiological pathways. MGG Mol Genet Genomics 266:821–826

    Article  CAS  Google Scholar 

  15. 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 

  16. Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of l-galactose dehydrogenase in the Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated l-galactose synthesis. Plant J 30:541–553

    Article  PubMed  CAS  Google Scholar 

  17. Giovannucci E, Ascherio A, Rimm E, Stampfer M, Colditz G, Willett W (1995) Intake of carotenoids and retinol in relationship to risk of prostate cancer. J Natl Cancer Inst 87:1767–1776

    Article  PubMed  CAS  Google Scholar 

  18. Giuliano G, Aquilani R, Dharmapuri S (2000) Metabolic engineering of plant carotenoids. Trends Plant Sci 5:406–409

    Article  PubMed  CAS  Google Scholar 

  19. Jones C, Mes P, Myers J (2003) Characterization and inheritance of the anthocyanin fruit (Aft) tomato. J Hered 94:449–456

    Article  PubMed  CAS  Google Scholar 

  20. Kahkonen MP, Hopia AI, Vuorela HJ, Rauha JP, Pihlaja K, Kujala TS, Heinonen M (1999) Antioxidant activity of plant extracts containing phenolic compounds. J Agric Food Chem 47:3954–3962

    Article  PubMed  CAS  Google Scholar 

  21. Khachik F, Carvalho L, Bernstein PS, Muir GJ, Zhao DY, Katz NB (2002) Chemistry, distribution, and metabolism of tomato carotenoids and their impact on human health. Exp Biol Med (Maywood) 227:845–851

    CAS  Google Scholar 

  22. Ku HM, Doganlar S, Chen KY, Tanksley SD (1999) The genetic basis of pear-shaped tomato fruit. Theor Appl Genet 99:844–850

    Article  CAS  Google Scholar 

  23. Lavelli V, Peri C, Rizzolo A (2000) Antioxidant activity of tomato products as studied by model reactions using xanthine oxidase, myeloperoxidase, and copper-induced lipid peroxidation. J Agric Food Chem 48:1442–1448

    Article  PubMed  CAS  Google Scholar 

  24. Lissi E, Salim-Hanna M, Pascual C, Del CMD (1995) Evaluation of total antioxidant potential (TRAP) and total antioxidant reactivity from luminol-enhanced chemiluminescence measurements. Free Radic Biol Med 18:153–158

    Article  PubMed  CAS  Google Scholar 

  25. Liu Y-S, Gur A, Ronen G, Causse M, Damidaux R, Buret M, Hirschberg J, Zamir D (2003) There is more to tomato fruit colour than candidate carotenoid genes. Plant Biotechnol J 1:195–207

    Article  PubMed  CAS  Google Scholar 

  26. Luwe MWF, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves. Plant Physiol (Rockville) 101:969–976

    CAS  Google Scholar 

  27. Martinez-Valverde I, Periago MJ, Provan G, Chesson A (2002) Phenolic compounds, lycopene and antioxidant activity in commercial varieties of tomato (Lycopersicum esculentum). J Sci Food Agric 82:323–330

    Article  CAS  Google Scholar 

  28. Miller JC, Tanksley SD (1990) Effect of different restriction enzymes, probe source, and probe length on detecting restriction fragment length polymorphism in tomato. Theor Appl Genet 80:385–389

    CAS  Google Scholar 

  29. Minoggio M, Bramati L, Simonetti P, Gardana C, Lemoli L, Santangelo E, Mauri PL, Spigno P, Soressi GP, Pietta PG (2003) Polyphenol pattern and antioxidant activity of different tomato lines and cultivars. Nutr metab 47:64–69

    Article  CAS  Google Scholar 

  30. Mittova V, Guy M, Tal M, Volokita M (2002a) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: increased activities of antioxidant enzymes in root plastids. Free Radic Res 36:195–202

    Article  PubMed  CAS  Google Scholar 

  31. Mittova V, Tal M, Volokita M, Guy M (2002b) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400

    Article  PubMed  CAS  Google Scholar 

  32. Monforte AJ, Friedman E, Zamir D, Tanksley SD (2001) Comparison of a set of allelic QTL-NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm utilization. Theor Appl Genet 102:572–590

    Article  CAS  Google Scholar 

  33. Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, De Vos CHR, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474

    Article  PubMed  CAS  Google Scholar 

  34. Olson JA (1989) Provitamin A function of carotenoids: the conversion of beta-carotene into vitamin A. Am J Clin Nutr 64:195–108

    Google Scholar 

  35. Ou B, Huang D, Hampsch-Woodill M, Flanagan JA, Deemer EK (2002) Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: a comparative study. J Agric Food Chem 50:3122–3128

    Article  PubMed  CAS  Google Scholar 

  36. Pan Q, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    PubMed  CAS  Google Scholar 

  37. Proteggente AR, Pannala AS, Paganga G, Van Buren L, Wagner E, Wiseman S, Van De Put F, Dacombe C, Rice-Evans CA (2002) The antioxidant activity of regularly consumed fruit and vegetables reflects their phenolic and vitamin C composition. Free Radic Res 36:217–233

    Article  PubMed  CAS  Google Scholar 

  38. Reto MP, Asins MJ, Carbonell EA (1993) Genetic variability in Lycopersicon species and their genetic relationships. Theor Appl Genet 86:113–120

    Google Scholar 

  39. Rick CM (1974) High soluble-solids content in large-fruited tomato lines derived from a wild green-fruited species. Hilgardia 42:493–510

    Google Scholar 

  40. Rick CM, Tanksley SD (1983) Isozyme monitoring of genetic variation in Lycopersicon. In: Liss A (ed) Isozymes: current topics in biological and medical research. vol 11. pp 269–284

  41. Romer S, Fraser PD, Kiano JW, Shipton CA, Misawa N, Schuch W, Bramley PM (2000) Elevation of the provitamin A content of transgenic tomato plants. Nat Biotechnol 18:666–669

    Article  PubMed  CAS  Google Scholar 

  42. Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107

    Article  PubMed  CAS  Google Scholar 

  43. Ronen G, Cohen M, Zamir D, Hirschberg J (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J 17:341–351

    Article  PubMed  CAS  Google Scholar 

  44. 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 

  45. Shalata A, Tal M (1998) The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:169–174

    Article  CAS  Google Scholar 

  46. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagent. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  48. Taungbodhitham AK, Jones GP, Wahlqvist ML, Briggs DR (1998) Evaluation of extraction method for the analysis of carotenoids in fruits and vegetables. Food Chem 63:577–584

    Article  CAS  Google Scholar 

  49. Vinson J, Hao Y, Su X, Zubik L (1996) Phenol antioxidant quantity and quality in foods: vegetables. J Agric Food Chem 46:3630–3634

    Article  Google Scholar 

  50. Wang H, Cao G, Prior RL (1996) Total antioxidant capacity of fruits. J Agric Food Chem 44:701–705

    Article  CAS  Google Scholar 

  51. Willcox JK, Catignani GL, Lazarus S (2003) Tomatoes and cardiovascular health. Crit Rev Food Sci Nutr 43:1–18

    Article  PubMed  CAS  Google Scholar 

  52. Zapata S, Dufour J-P (1992) Ascorbic, dehydroascorbic and isoascorbic acid simultaneous determinations by reverse phase ion interaction HPLC. J Food Sci 57:506–511

    Article  CAS  Google Scholar 

  53. Zhang Y, Stommel JR (2000) RAPD and AFLP tagging and mapping of Beta (B) and Beta modifier (Mo-B), two genes which influence beta-carotene accumulation in fruit of tomato (Lycopersicon esculentum Mill.). Theor Appl Genet 100:368–375

    Article  CAS  Google Scholar 

  54. Zscheille F, Porter J (1947) Analytical methods for carotenes of Lycopersicon species and strains. Anal Chem 19:47–51

    Article  Google Scholar 

Download references

Acknowledgements

This work was support by Campbell Research and Development. MCR was supported in part by an Argentinean Council of Science (CONICET) scholarship. The authors thank Betty Hess-Pierce for her help with the ascorbate HPLC determinations, and Jessica Nguyen, Scott Dixon, Sarah Stuart, Kam Hon Hoi, Amanda Vlasveld, Arlen Abraham, Vasiliy Loscutoff, Celeste Powell, Anna Sinemus, Luna Phillips, Lorena Marquez, and Zack Robinson for their assistance in the field and/or laboratory.

Author information

Author notes

  1. M. Cecilia Rousseaux

    Present address: CRILAR (CONICET), Entre Rios y Mendoza s/n, 5301, Anillaco, La Rioja, Argentina

Authors and Affiliations

  1. Department of Plant Sciences, Mail Stop 3, University of California Davis, One Shield Ave, Davis, CA, 95616-8780, USA

    M. Cecilia Rousseaux, Carl M. Jones, Roger Chetelat, Alan Bennett & Ann Powell

  2. Campbell Research and Development, County Road 104, 28605, Davis, CA, 95616, USA

    Dawn Adams

Authors
  1. M. Cecilia Rousseaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carl M. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dawn Adams
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roger Chetelat
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alan Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ann Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Cecilia Rousseaux.

Additional information

Communicated by I. Paran

M. Cecilia Rousseaux and Carl M. Jones contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rousseaux, M.C., Jones, C.M., Adams, D. et al. QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111, 1396–1408 (2005). https://doi.org/10.1007/s00122-005-0071-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-005-0071-7

Keywords

Search

Navigation