Abstract
Epidemiological and clinical studies indicate that a steady dietary intake of bioavailable lycopene, a C40 carotenoid and potent natural antioxidant, may be associated with a decreased incidence of prostate cancer in humans. Since fresh tomatoes and processed tomato products represent approximately 85% of the average human’s dietary lycopene intake, the identification of novel genetic factors which regulate high fruit lycopene content in tomato is imperative for the improvement of nutritional quality in this commercially valuable specialty crop. To understand the genetic control of the extraordinarily high fruit lycopene content in an accession (LA2093) of the tomato wild species Solanum pimpinellifolium, a quantitative trait locus (QTL) mapping study was conducted using a recombinant inbred line (RIL) population of a cross between LA2093 and a cultivated tomato (S. lycopersicum) breeding line, NCEBR-1. The parental lines, F1 progeny, and F7-F10 RIL populations were grown in replicated field trials in four successive years and evaluated for lycopene content as well as several other traits, including fruit fresh weight, soluble solids content, pH of puree, and plant maturity. The lycopene content of ripe fruit was estimated using three methods: high-performance liquid chromatography (HPLC), spectrophotometry, and colorimetric assays. Based on these measurements, QTL were identified and compared across generations. Among the QTL identified for lycopene, two QTL, located on chromosomes 7 and 12, had very large effects and were consistent across generations. The genomic intervals in which these two QTL reside do not correspond to known map positions of carotenoid biosynthetic genes, indicating that these QTL may represent novel alleles with potentially important implications for tomato breeding as well as increased understanding of carotenoid accumulation in tomato. Several QTL were also identified for fruit weight, soluble solids content and plant maturity. The potential implications of these results for tomato crop improvement are discussed.
Similar content being viewed by others
References
Agarwal S, Rao AV (2000) Tomato lycopene and its role in human health and chronic diseases. Can Med Assoc J 163:739–744
Ashrafi H, Kinkade M, Foolad MR (2009) A new genetic linkage map of tomato based on a Solanum lycopersicum × S. pimpinellifolium RIL population displaying locations of candidate pathogen response genes. Genome 52:935–956
Bartley GE, Viitanen PV, Bacot KO, Scolnik PA (1992) A tomato gene expressed during fruit ripening encodes an enzyme of the cartenoid biosynthesis pathway. J Biol Chem 267:5036–5039
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
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
Chaib J, Lecomte L, Buret M, Causse M (2006) Stability over genetic backgrounds, generations and years of quantitative trait locus (QTLs) for organoleptic quality in tomato. Theor Appl Genet 112:934–944
Chen FQ, Foolad MR, Hyman J, St. Clair DA, Beelman 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 Breeding 5:283–299
Chen Y, Li F, Wurtzel ET (2010) Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol 153:66–79. doi:10.1104/pp.110.153916
Doganlar S, Frary A, Ku HM, Tanksley SD (2002) Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome 45:1189–1202
Dudley JW, Moll RH (1969) Interpretation and use of estimates of heritability and genetic variances in plant breeding. Crop Sci 9:257–261
FAO (2009) Tomato—crop water management. http://www.fao.org/landandwater/aglw/cropwater/tomato.stm. Accessed 12/01/2009
Faria MV, Maluf WR, Azevedo SMd, Andrade Junior VCd, Gomes LAA, Moretto P, Licursi V (2003) Yield and post-harvest quality of tomato hybrids heterozygous at the locialcobaça, old gold-crimson or high pigment. Genet Mol Res 2:317–327
Foolad MR (2007) Genome mapping and molecular breeding of tomato. Intl J Plant Genomics 2007:52. doi:10.1155/2007/64358
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
Frary A, Fulton TM, Zamir D, Tanksely SD (2004) Advance backcross QTL analysis of a Lycopersicon esculentum × L. pennellii cross and indentification of possible orthologs in the Solanaceae. Theor Appl Genet 108:485–496
Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265
Fray RG, Grierson D (1993) Molecular genetics of tomato fruit ripening. Trends Genet 9:438–443
Frey KJ, Horner T (1957) Heritability in standard units. Agron J 49:59–62
Fulton RM, 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 comparison with QTLs found in other wild species. Theor Appl Genet 95:881–894
Fulton TM, Grandillo S, Beck-Bunn T, Fridman E, Frampton AJ, Lopez J, Petiard V, Uhlig J, Zamir D, Tanksley SD (2000) Advance backcross QTL analysis of a Lycopersicon esculentum × Lycopersicon parviflorum cross. Theor Appl Genet 100:1025–1042
Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53:717–730
Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137:199–208. doi:10.1104/pp.104.051987
Goldman IL, Paran I, Zamir D (1995) Quantitative trait locus analysis of a recombinant inbred line population derived from Lycopersicon esculentum × 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
Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987
Hyman JR, Gaus J, Foolad MR (2004) A rapid and accurate method for estimating tomato lycopene content by measuring chromaticity values of fruit puree. J Am Soc Hort Sci 129:717–723
Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of {beta}-carotene and xanthophylls in plants. Plant Cell 14:333–342. doi:10.1105/tpc.010303
Jatoi A, Burch P, Hillman D, Vanyo JM, Dakhil S, Nikcevich D, Rowland K, Morton R, Flynn PJ, Young C, Tan W (2007) A tomato-based, lycopene-containing intervention for androgen-independent prostate cancer: Results of a phase II study from the north central cancer treatment group. Urology 69:289–294
Kao C-H, Zeng Z-B, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216
Kucuk O (2002) Lycopene in the treatment of prostate cancer. Pure Appl Chem 74:1443–1450
Lecomte L, Duffé P, Buret M, Servin B, Hospital F, Causse M (2004) Marker-assisted introgression of five QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. Theor Appl Genet 109:658–668
Lippman Z, Tanksley SD (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics 158
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. doi:10.1046/j.1467-7652.2003.00018.x
Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902
Lower RL, Thompson AE (1967) Inheritance of acidity and solids content of small-fruited tomatoes. Proc Am Soc Hort Sci 91:486–494
MacArthur JW, Butler L (1938) Size inheritance and geometric growth processes in the tomato fruit. Genetics 23:253–268
Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11:145–157
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
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
Rao AV, Rao LG (2007) Carotenoids and human health. Pharmacol Res 55:207–216
Rick CM (1974) High soluble-solids content in large-fruited tomato lines derived from a wild green-fruited species. Hilgardia 42:493–510
Rick CM (1982) The potential of exotic germplasm for tomato improvement. In: Vasil IK, Scowcroft WR, Freys KJ (eds) Plant improvement and somatic cell genetics. Academic Press, New York, pp 1–28
Ronen G, Cohen M, Zamir D, Hirschberg J (1999) Regulation of carotenoids 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. doi:10.1046/j.1365-313X.1999.00381.x
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. doi:10.1073/pnas.190177497
Rousseaux M, Jones C, 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
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
Stevens MA (1986) Inheritance of tomato fruit quality components. Plant Breed Rev 4:273–311
Stevens MA, Kader AA, Albright M (1979) Potential for increasing tomato flavor via increased sugar and acid content breeding. J Am Soc Hort Sci 104:40–42
Suresh Kumar G, Deepa T, Sushma S, Sujata J, Nabanita H, Shambhu DV (2003) Lycopene attenuates oxidative stress induced experimental cataract development: an in vitro and in vivo study. Nutrition (Burbank, Los Angeles County, Calif) 19:794–799
Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. The Plant Cell Online 16:S181–S189. doi:10.1105/tpc.018119
Tanksley SD, Hewitt J (1988) Use of molecular markers in breeding for soluble solids content in tomato—a re-examination. Theor Appl Genet 75:811–823
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
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
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 Tuinen A, Koornneef M, Cordonnier-Pratt M, Pratt L, Verkerk R, Zabel P (1997) The mapping of phytochrome genes and photomorphogenic mutants of tomato. Theor Appl Genet 94:115–122
Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Heredity 93:77–78
Wang S, Basten CJ, Weir BS, Zeng Z-B (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh
Wann EV (1995) Reduced plant growth in tomato mutants high pigment and dark green partially overcome by gibberellin. Hortscience 30:379
Wu K, Erdman JW, Schwartz SJ, Platz EA, Leitzmann M, Clinton SK, DeGroff V, Willett WC, Giovannucci E (2004) Plasma and dietary carotenoids, and the risk of prostate cancer. Cancer Epidemiol Biomarkers Prev 13:260–269
Yen HC (1997) The tomato high-pigment (hp) locus maps to chromosome 2 and influences plastome copy number and fruit quality. Theor Appl Genet 95:1069–1079
Zeng ZB (1993) Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci USA 90:10972–10976
Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Acknowledgments
This research was supported in part by Agricultural Research Funds administered by the Pennsylvania Department of Agriculture, the Pennsylvania Vegetable Marketing and Research Program, and the College of Agricultural Sciences at the Pennsylvania State University. The authors graciously thank Dr. Randolph Gardner for providing seed of breeding line NCEBR-1, and all Penn State staff and undergraduates who helped with field experiments and data collection.
Author information
Authors and Affiliations
Corresponding author
Additional information
Hamid Ashrafi and Matthew P. Kinkade contributed equally to this research.
Rights and permissions
About this article
Cite this article
Ashrafi, H., Kinkade, M.P., Merk, H.L. et al. Identification of novel quantitative trait loci for increased lycopene content and other fruit quality traits in a tomato recombinant inbred line population. Mol Breeding 30, 549–567 (2012). https://doi.org/10.1007/s11032-011-9643-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-011-9643-1