Skip to main content
SpringerLink
Log in

Characterization and mapping of a QTL derived from Solanum habrochaites associated with elevated rutin content (quercetin-3-rutinoside) in tomato

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Consumption of flavonoids found in fruits and vegetables is linked to beneficial health outcomes. Tomato is among the most widely consumed and economically important vegetables worldwide and improvement of the nutrient content could lead to significant health benefits. Rutin, (quercetin-3-rutinoside), the main flavonol in tomato fruit, is confined to the peel. Rutin synthesis is limited by low expression of chalcone isomerase, the enzyme catalyzing the conversion of naringenin chalcone to naringenin quercetin. The wild tomato species Solanum habrochaites is a major source of new alleles to improve cultivated tomato (Solanum lycopersicum). AVRDC—The World Vegetable Center identified introgression line (IL) LA3984 containing a segment of S. habrochaites on chromosome 5 expressing high levels of rutin in full red ripe fruit. An AVRDC high rutin tomato line evaluated for 2 years and two seasons in Taiwan produced mean rutin content about four- to five-fold greater than the mean of all entries and about 11–12 times higher than the commercial fresh market and processing tomato cultivars. The quantitative trait locus (QTL) conditioning high rutin content was mapped to a 0.42 Mb segment on chromosome 5 flanked by markers c2_At3g55120/TaqI and ch05-4.883/ApaLI. Marker c2_Atg55120 overlaps with the chalcone-flavonone isomerase gene Solyc05g10320, and a second chalcone-flavonone isomerase gene is located 3,000 bp upstream from c2_At3g551220. Results of this project will facilitate breeding of high flavonoid tomato lines.

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.

Fig. 1

Similar content being viewed by others

References

  • Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Dominguez E, Wang Z, De Vos RCH, Jetter R, Schreiber L, Heredia A, Rogachev I, Aharoni A (2009) Fruit-surface flavonoid accumulation in tomato is controlled by a SIMYB12-regulated transcriptional network. PLoS Genet 5:1–23

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bernacchi D, Beck-Bunn T, Emmaty D, Eshed Y, Inai S, Lopez J, Petiard V, Sayama H, Uhlig J, Zamir D, Tanksley S (1998b) Advanced backcross QTL analysis of tomato. II. Evaluation of near-isogenic lines carrying single-donor introgressions for desirable wild QTL-alleles derived from L. hirsutum and L. pimpinellifolium. Theor Appl Genet 97:170–180

    Article  CAS  Google Scholar 

  • Bovy A, de Vos R, Kemper M, Schijlen E, Almenar Pertejo M, Muir S, Collins G, Robinson S, Verhoeyen M, Highes S, Santos-Buelga C, van Tunen A (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bovy A, Schijlen E, Hall RD (2007) Metabolic engineering of flavonoids in tomato (Solanum lycopersicum): the potential for metabolomics. Metabolomics 3:399–412

    Article  CAS  Google Scholar 

  • Chetelat RT (2000) TGRC stock list XII. Introgression lines. 2. L. hirsutum introgression lines. Rept Tomato Genet Coop 50:74–77

    Google Scholar 

  • Commenges D, Scotet V, Renaud S, Jacqmin-Gadda H, Barberger-Gateau P, Dartigues JF (2000) Intake of flavonoids and risk of dementia. Eur J Epidemiol 16:357–363

    Article  CAS  PubMed  Google Scholar 

  • Dao TTH, Linthorst HJM, Verporte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Jong WS, Eannetta NT, De Jong DM, Bodis M (2004) Candidate gene analysis of anthocyanin pigmentation loci in the Solanaceae. Theor Appl Genet 108:423–432

    Article  PubMed  Google Scholar 

  • de Leeuw PW, Bast A (2009) Tomato extract for hypertension? Editorial to The effects of natural antioxidants from tomato extract in treated but uncontrolled hypertensive patients. Cardiovasc Drugs Ther 23:107–108

    Article  PubMed  Google Scholar 

  • Eshed Y, Zamir D (1994) A genome library of Lycopersicon pennellii in L. esculentum: a tool for finemapping genes. Euphytica 79(3):175–179

    Article  CAS  Google Scholar 

  • Eshed Y, Abu-Abied M, Saranga Y, Zamir D (1992) Lycopersicon esculentum lines containing small overlapping introgressions from L. pennellii. Theor Appl Genet 83:1027–1034

    Article  CAS  PubMed  Google Scholar 

  • Frankel EN, Kanner J, German JB, Parks E, Kinsella JE (1993) Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 341:454–457

    Article  CAS  PubMed  Google Scholar 

  • Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209

    Article  CAS  Google Scholar 

  • Grandillo S, Chetelat R, Knapp S, Spooner D, Peralta I, Cammareri M, Perez O, Termolino P, Termolino P, Tripodi P, Chiusano ML, Ercolano MR, Frusciante L, Monti L, Pignone D (2011) Solanum sect. Lycopersicon. In: Cole C (ed) Wild crop relatives: genomic and breeding resources, vegetables. Springer-Verlag, Berlin, pp 129–215

    Chapter  Google Scholar 

  • Hanson PM, Yang RY, Wu J, Chen JT, Ledesma D, Tsou SCS, Lee TC (2004) Variation for antioxidant activity and antioxidants in tomato. J Amer Soc Hort Sci 129:704–711

    CAS  Google Scholar 

  • Hanson P, Green SK, Kuo G (2006) Ty-2 gene on chromosome 11 conditioning geminivirus resistance in tomato. Tomato Genetics Coop Rep 56:17–18

    Google Scholar 

  • Hanson P, Sitathani K, Sadashiva AT, Yang R-Y, Graham E, Ledesma D (2007) Performance of Solanum habrochaites LA1777 introgression line hybrids for marketable tomato fruit yield in Asia. Euphytica 158:167–178

    Article  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  CAS  PubMed  Google Scholar 

  • Hertog MGL, Feskens EJ, Kromhout D (1997) Antioxidant flavonols and coronary heart disease risk. Lancet 349:699

    Article  CAS  PubMed  Google Scholar 

  • Hollman PCH, Hertog MGL, Katan MB (1996) Role of dietary flavonoids in protection against cancer and coronary heart disease. Biochem Soc Trans 24:785–789

    CAS  PubMed  Google Scholar 

  • Huxley RR, Neil HAW (2003) The relation between dietary flavonol intake and coronary heat disease mortality: a meta-analysis of prospective cohort studies. Eur J Clin Nutr 57:904–908

    Article  CAS  PubMed  Google Scholar 

  • Ji Y, Schuster DJ, Scott JW (2007) Ty-3, a begomovirus resistance locus near the tomato yellow leaf curl virus resistance locus Ty-1 on chromosome 6 of tomato. Mol Breed 20:271–284

    Article  CAS  Google Scholar 

  • Jones CM, Mes P, Myers JR (2003) Characterization and inheritance of the Anthocyanin fruit (Aft) tomato. J Hered 94:449–456

    Article  CAS  PubMed  Google Scholar 

  • Kabelka E, Yang W, Francis DM (2004) Improved fruit color within an inbred backcross line derived from Lycopersicon esculentum and L. hirsutum involves the interaction of loci. J Amer Soc Hort Sci 129:250–257

    CAS  Google Scholar 

  • Kneckt P, Jarvinen R, Seppaanen R, Heliovaara M, Teppi L, Pukkala E, Aromaa A (1997) Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. Am J Epidem 146:223–230

    Article  Google Scholar 

  • Le Gall G, DuPont MS, Mellon FA, Davis AL, Collins GJ, Verhoeyen ME, Colquhoun IL (2003) Characterization and content of flavonoid glycosides in genetically modified tomato (Lycopersicon esculentum) fruit. J Agric Food Chem 51:2438–2446

    Article  PubMed  Google Scholar 

  • Levin I, Lalazar A, Bar M, Schaffer AA (2004) Non GMO fruit factories: strategies for modulating metabolic pathways in tomato fruit. Ind Crop Prod 20:29–36

    Article  CAS  Google Scholar 

  • Ott RL, Longnecker, M (2001). Statistical methods and data analysis. 5th ed. Wadsworth Group, Duxbury

  • Monforte AJ, Tanksley SD (2000a) Development of a near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum background: a tool for gene mapping and gene discovery. Genome 43:803–813

    Article  CAS  PubMed  Google Scholar 

  • Monforte AJ, Tanksley SD (2000b) Fine mapping of a quantitative trait locus (QTL) from Lycopersicin hirsutum chromosome 1 affecting fruit characteristics and agronomic traits: breaking linkage among QTLs affecting different traits and dissection of heterosis for yield. Theor Appl Genet 100:471–479

    Article  CAS  Google Scholar 

  • 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 dramatically increased levels of flavonols. Nat Biotechnol 19:470–474

    Article  CAS  PubMed  Google Scholar 

  • Peet MM (1992) Fruit cracking in tomato. HortTechnology 2:216–223

    Google Scholar 

  • Rick CM, Cisneros P, Chetelat RT, DeVerna JW (1993) Abg–a gene on chromosome 10 for purple fruit derived from S. lycopersicoides. Rept Tomato Genet Coop 44:29–30

    Google Scholar 

  • SAS Institute Inc. (2000) SAS OnlineDoc®, Version 8. Cary, NC

  • Schijlen EGWM, de Vos CHR, Martens S, Jonker HN, Rosin FM, Molthoff JW, Tikunov YM, Angenent GC, van Tunen AJ, Bovy AG (2007) RNAi silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol 144:1520–1530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sheskin D (2004) Handbook of parametric and nonparametric statistical procedures. 3rd ed. Chapman and Hall/CRC

  • Simonetti P, Gardana C, Riso P, Mauri P, Pietta P, Porinni M (2005) Glycosylated flavonoids from tomato puree are bioavailable in humans. Nutr Res 25:717–726

    Article  CAS  Google Scholar 

  • Sol Genomics Network (2013) http://solgenomics.net/. Accessed Nov. 28 2013

  • Stewart AJ, Bozonnet S, Mullen W, Jenkins GI, Lean ME, Crozier A (2000) Occurrence of flavonols in tomatoes and tomato-based products. J Agric Food Chem 48:2663–2669

    Article  CAS  PubMed  Google Scholar 

  • Stommel JR, Haynes KG (1993) Genetic control of fruit sugar accumulation in a Lycopersicon esculentum × L. hirsutum cross. J Amer Soc Hort Sci 118:859–863

    CAS  Google Scholar 

  • Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet 92:191–203

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Tomes ML, Quakenbush FW, McQuistan M (1954) Modification and dominance of the gene governing formation of high concentrations of beta-carotene in the tomato. Genetics 39:810–817

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vauzour D, Vafeiadou K, Rodriguez-Mateos A, Rendeiro C, Spencer JPE (2008) The neuroprotective potential of flavonoids: a multiplicity of effects. Genes Nutr 3:115–126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, de Vos CHR, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106

    Article  CAS  PubMed  Google Scholar 

  • Wann EV (1997) Tomato germplasm lines T4065, T4099, T5019, and T5020 with unique genotypes that enhance fruit quality. HortScience 32:747–748

    Google Scholar 

  • Willits MG, Kramer CM, Prata RTN, De Luca V, Potter BG, Steffens JC, Graser G (2005) Utilization of the genetic resources of wild tomato species to create a nontransgenic high flavonoid tomato. J Agric Food Chem 53:1231–1236

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223

    Article  CAS  PubMed  Google Scholar 

  • Yao LH, Jiang YM, Shi J, Tomás-Barberán FA, Datta N, Singanusong R, Chen SS (2004) Flavonoids in food and their health benefits. Plant Foods Hum Nutr 59:113–122

    Article  CAS  PubMed  Google Scholar 

  • Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Maureen Mecozzi for editing the manuscript and the CM Rick Tomato Genetics Resources Center at the University of California-Davis for providing seeds of the introgression lines. Financial support from the Federal Ministry for Economic Cooperation and Development, Germany, project number 03.7860.4–001.00 is gratefully acknowledged.

Author information

Authors and Affiliations

  1. AVRDC – The World Vegetable Center, PO Box 42, Shanhua, Tainan, 74199, Taiwan

    Peter Hanson, Roland Schafleitner, Shu-Mei Huang, Chee-Wee Tan, Dolores Ledesma & Ray-Yu Yang

  2. 135, Jalan Seri Impian 4/3, Taman Seri Impian, 86000, Kluang, Johor, Malaysia

    Chee-Wee Tan

Authors
  1. Peter Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roland Schafleitner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shu-Mei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chee-Wee Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dolores Ledesma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ray-Yu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Hanson.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hanson, P., Schafleitner, R., Huang, SM. et al. Characterization and mapping of a QTL derived from Solanum habrochaites associated with elevated rutin content (quercetin-3-rutinoside) in tomato. Euphytica 200, 441–454 (2014). https://doi.org/10.1007/s10681-014-1180-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-014-1180-7

Keywords

Search

Navigation