Skip to main content
Log in

QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium

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

Abstract

Molecular markers were used to map and characterize quantitative trait loci (QTLs) for several characters of agronomic and biological importance in an interspecific backcross of tomato. The parents of the cross were an elite processing inbred Lycopersicon esculentum cv ‘M82-1-7’ and the closely related red-fruited wild species L. pimpinellifolium (LA1589). A total of 257 BC1 plants were grown under field conditions in Ithaca, New York and scored for 19 quantitative traits. A genetic linkage map was constructed for the same population using 115 RFLP, 3 RAPD and 2 morphological markers that spanned 1,279 cM of the tomato genome with an average interval length of 10.7 cM. A minimum of 54 putatively significant QTLs (P<0.001; LOD> 2.4) were detected for all characters with a range of 1–7 QTLs detected per character. Of the total 54 QTLs 11% had alleles with effects opposite to those predicted by the parental phenotypes. The percentage of phenotypic variation associated with single QTLs ranged from 4% to 47%. Multilocus analysis showed that the cumulative action of all QTLs detected for each trait accounted for 12–59% of the phenotypic variation. The difference in fruit weight was controlled largely by a single major QTL (fw2.2). Digenic epistasis was not evident. Several regions of the genome (including the region near sp on chromosome 6) showed effects on more than one trait. Implications for variety improvement and inferences about the domestication of the cultivated tomato are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Banerjee MK, Kalloo (1989) The inheritance of earliness and fruit weight in crosses between cultivated tomatoes and two wild species of Lycopersicon. Plant Breed 102:148–152

    Google Scholar 

  • Bonierbale MW, Plaisted RL, Pineda O, Tanksley SD (1994) QTL analysis of trichome-mediated insect resistance in potato. Theor Appl Genet 87:973–987

    Google Scholar 

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

    Google Scholar 

  • Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    CAS  PubMed  Google Scholar 

  • Doebley J, Bacigalupo A, Stec A (1994) Inheritance of kernel weight in two maize-teosinte hybrid populations: implications for crop evolution. J Hered 85:191–195

    Google Scholar 

  • East EM (1915) Studies on size inheritance in Nicotiana. Genetics 1:164–176

    Google Scholar 

  • Edwards MD, Stuber CW, Wendel JF (1987) Molecular-markerfacilitated investigations of quantitative-trait loci in maize. I. Numbers, genomic distribution and types of gene action. Genetics 116:113–125

    CAS  PubMed  Google Scholar 

  • Emery GC, Munger HM (1970) Effect of inherited differences in growth habit on fruit size and soluble solids in tomato. J Am Soc Hortic Sci 95:410–412

    Google Scholar 

  • 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 QTLs. Genetics 141:1147–1162

    CAS  PubMed  Google Scholar 

  • Fatokun CA, Menancio-Hautea DI, Danesh D, Young ND (1992) Evidence for orthologous seed weight genes in cowpea and mung bean based on RFLP mapping. Genetics 132:841–846

    Google Scholar 

  • Fogle HW, Currence TM (1950) Inheritance of fruit weight and earliness in a tomato cross. Genetics 35:363–380

    Google Scholar 

  • Geldermann H (1975) Investigations on inheritance of quantitative characters in animals by gene markers. I. Methods. Theor Appl Genet 46:319–330

    Google Scholar 

  • Goldenberg JB, von der Pahleen A (1966) Genetic and phenotypic correlation between weight and dry matter content of tomato fruits and their heritabilities. Bol Genet 2:1–15

    Google Scholar 

  • Grandillo S, Tanksley SD (1996) Genetic analysis of RFLPs, GATA microsatellites and RAPDs in a cross between L.esculentum and L. pimpinellifolium. Theor Appl Genet 92:957–965

    Google Scholar 

  • Hayes PM, Blake TK, Chen THH, Tragoonrung S, Chen F, Pan A, Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare) chromosome 7 associated with components of winter hardiness. Genome 36:66–71

    Google Scholar 

  • Houghtaling HB (1935) A developmental analysis of size and shape in tomato fruits. Bull Torrey Bot Club 62:243–252

    Google Scholar 

  • Humphrey LM (1937) A cytological and morphological analysis of tomato species. Cytologia 8:306–318

    Google Scholar 

  • Ibarbia EA, Lambeth VN (1969) Inheritance of soluble solids in a large/small-fruited tomato cross. J Am Soc Hortic Sci 94:496–498

    Google Scholar 

  • Ibarbia EA, Lambeth VN (1971) Tomato fruit size and quality interrelationships. J Am Soc Hortic Sci 96:199–201

    Google Scholar 

  • Johanssen W (1909) Elemente der exakten Erblichkeitslehre. Fisher, Jena

    Google Scholar 

  • Khalf-Allah AM, Pierce LC (1963) A comparison of selection methods for improving earliness, fruit size and yield in the tomato. Proc Am Soc Hortic Sci 82:414–419

    Google Scholar 

  • Khalf-Allah AM, Pierce LC (1964) The effect of sib-mating on variation and selection of quantitative characters in the tomato. Proc Am Soc Hortic Sci 85:471–477

    Google Scholar 

  • Keim P, Diers BW, Olson TC, Shoemaker RC (1990) RFLP mapping in soybean: association between marker loci and variation in quantitative traits. Genetics 126:735–742

    Google Scholar 

  • Kemble JM, Gardner RG (1992) Inheritance of shortened fruit maturation in the cherry tomato Cornell 871213–1 and its relation to fruit size and other components of earliness. J Am Soc Hortic Sci 117:646–650

    Google Scholar 

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

    Google Scholar 

  • Ladizinsky G (1985) Founder effect in crop-plant evolution. Econ Bot 39:191–199

    Google Scholar 

  • Lambeth VN, Straten EF, Fields ML (1966) Fruit quality attributes of 250 foreign and domestic tomato accessions. Mo Res Bull 908

  • Lande R (1983) The response to selection on major and minor mutations affecting a metrical trait. Heredity 50:47–65

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    CAS  PubMed  Google Scholar 

  • Leonards-Schippers C, Gieffers W, Schäfer-Pregl R, Ritter E, Knapp SJ, Salamini F, Gebhardt C (1994) Quantitative resistance to Phytophtora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77

    Google Scholar 

  • Lincoln S, Daly M, Lander E (1992) Mapping genes controlling quantitative traits with MAPMAKER/QTL 1.1 Whitehead Institute Technical Report, 2nd edn

  • Lindhout P, Van Heusden S, Pet G, Van Ooijen JW, Sandbrink H, Verkerk R, Vrielink R, Zabel P (1994) Perspectives of molecular marker assisted breeding for earliness in tomato. Euphytica 79: 279–286

    Google Scholar 

  • Lindstrom EW (1927) The inheritance of ovate and related shapes of tomato fruits. J Agric Res 34: 961–985

    Google Scholar 

  • Lindstrom EW (1935) Segregation of quantitative genes in tetraploid tomato hybrids as evidence for dominance relations of size characters. Genetics 20:1–11

    Google Scholar 

  • Luckwill LC (1943) The genus Lycopersicon, an historical, biological, and taxonomic survey of the wild and cultivated tomatoes. Aberdeen University Studies, Scotland, No. 120

  • MacArthur JW (1928) Linkage studies with the tomato II. Three linkage groups. Genetics 13:410–420

    Google Scholar 

  • MacArthur JW, L Butler (1938) Size inheritance and geometric growth processes in the tomato fruit. Genetics 23:253–268

    Google Scholar 

  • Manly KF (1993) A Macintosh program for storage and analysis of experimental genetic mapping data. Mamm Genome 4: 303–313

    Google Scholar 

  • Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphism associated with water use efficiency in tomato. Science 243:1725–1728

    Google Scholar 

  • Miller JC, Tanksley SD (1990) RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor Appl Genet 80:437–448

    CAS  Google Scholar 

  • Nelson CJ (1994) Molecular mapping in bread wheat. PhD thesis. Cornell University. Ithaca, N.Y.

    Google Scholar 

  • Nienhuis J, Helentjaris T, Slocum M, Ruggero B, Schaefer A (1987) Restriction fragment length polymorphism analysis of loci associated with insect resistance in tomato. Crop Sci 27:797–803

    CAS  Google Scholar 

  • Nilsson-Ehle H (1909) Kreuzunguntersuchungen an Hafer und Weizen. Lunds. Univ Aarskz NF 5:1–122

    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  PubMed  Google Scholar 

  • Paterson AH, De Verna JW, Lanini B, Tanksley SD (1990) Fine mapping of quantitative trait loci using selected overlapping recombinant chromosomes, in an interspecies cross of tomato. Genetics 124:735–742

    Google Scholar 

  • Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinovitch 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

    Google Scholar 

  • Pierce LC, Currence TM (1959) The efficiency of selecting for earliness, yield, and fruit size in a tomato cross. Proc Am Soc Hortic Sci 73:294–304

    Google Scholar 

  • Powers L (1955) Components of variance method and partitioning method of genetic analysis applied to weight per fruit of tomato hybrid and parental populations. US Dep Agric Tech Bull 1131:1–64

    Google Scholar 

  • Powers L, Locke LF, Garret JC (1950) Partitioning method of genetic analysis applied to quantitative characters of tomato crosses. US Dep Agric Tech Bull 998:1–56

    Google Scholar 

  • Rick CM (1958) The role of natural hybridization in the derivation of cultivated tomatoes in western South America. Econ Bot 12: 346–367

    Google Scholar 

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

    Google Scholar 

  • Rick CM (1976) Tomato Lycopersicon esculentum (Solanaceae). In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 268–273

    Google Scholar 

  • Rick CM (1982) The Potential of exotic germplasm for tomato improvement. In: Vasil IK, Scowcroft WR, Frey KJ (eds) Plant improvement and somatic cell genetics. Academic Press, New York, pp 478–495

    Google Scholar 

  • SAS Institute (1988) SAS users guide: statistics. SAS Institute, Cary, N.C.

    Google Scholar 

  • SAS Institute (1989) JMP users guide: Version 3.0 of JMP. SAS Institute, Cary, N.C.

    Google Scholar 

  • Schön CC, Melchinger AE, Boppenmaier J, Brunklaus-Jung E, Herrmann RG, Seitzer JF (1994) RFLP mapping in maize: quantitative trait loci affecting testcross performance of elite European flint lines. Crop Sci 34:378–389

    Google Scholar 

  • Simmonds NW (1976) Evolution of crop plants. Longman, London New York

    Google Scholar 

  • Stevens MA, Rudich J (1978) Genetic potential for overcoming physiological limitations on adaptability, yield, and quality in the tomato. Hortic Sci 13:673–678

    Google Scholar 

  • Stubbe H (1971) Weitere evolutionsgenetische Unterschungen in der Gattung Lycopersicon. Biol Zbl 90:545–559

    Google Scholar 

  • Stuber CW, Edwards MD, Wendel JF (1987) Molecular markefacilitated investigations of quantitative trait loci in maize. II. Factors influencing yield and its component traits. Crop Sci 27:639–648

    Google Scholar 

  • Stuber CW, Lincoln SE, Wolff DW, Helentjaris T, Lander ES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132:823–839

    CAS  PubMed  Google Scholar 

  • Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27: 205–233

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD, Hewitt J (1988) Use of molecular markers in breeding for soluble solids in tomato-a re-examination. Theor Appl Genet (1988) 75:811–823

    Google Scholar 

  • Tanksley SD, Medina-Filho H, Rick CM (1982) Use of naturallyoccurring enzyme variation to detect and map genes controlling quantitative traits in an interspecific backcross of tomato. Heredity 49:11–25

    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  Google Scholar 

  • Wang G, Mackill DJ, Bonman JM, McCouch SR, Champoux MC, Nelson RJ (1994) RFLP mapping of genes conferring complete and partial resistance to blast in a durably resistant rice cultivar. Genetics 136:1421–1434

    CAS  PubMed  Google Scholar 

  • Wang ZY, Second G, Tanksley SD (1992) Polymorphism and phylogenetic relationships among species in the genus Oryzae as determined by analysis of nuclear RFLPs. Theor Appl Genet 83:565–581

    Google Scholar 

  • Weller JI, Soller M, Brody T (1988). Linkage analysis of quantitative traits in an interspecific cross of tomato (Lycopersicon esculentum x Lycopersicon pimpinellifolium) by means of genetic markers. Genetics 118:329–339

    Google Scholar 

  • Yeager AF (1937) Studies on the inheritance and development of fruit size and shape in the tomato. J Agric Res 55:141–152

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by M. Koorneef

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grandillo, S., Tanksley, S.D. QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium . Theoret. Appl. Genetics 92, 935–951 (1996). https://doi.org/10.1007/BF00224033

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00224033

Key words

Navigation