, Volume 184, Issue 2, pp 165–179 | Cite as

RETRACTED ARTICLE: A reexamination of molecular markers for use in marker-assisted breeding in tomato

  • Dilip R. Panthee
  • Majid R. Foolad


Molecular markers have been used for identification and mapping of genes and QTLs for numerous agriculturally important traits in tomato, including resistance/tolerance to biotic and abiotic stresses and fruit- and flower-related characteristics. However, the extent to which markers have been utilized in tomato breeding programs has not been clearly determined. A review of the literature indicated that the utility of most markers for use in tomato breeding programs have not been verified. Many markers are not validated across tomato genotypes or are not polymorphic within tomato breeding populations. In this study, we examined the utility of available markers for several major disease resistance traits in tomato by testing them in a number of breeding lines and commercial cultivars with known resistance/susceptibility responses. While several markers were validated, others needed PCR optimization for successful amplifications or were not informative in the genotypes used. Specifically, of the 37 markers examined 19 (~51%) were informative, including markers for resistance to Fusarium wilt, late blight, bacterial wilt, tomato mosaic virus, tomato spotted wilt virus, and root knot nematodes. It appears that many of the available markers may need to be further refined or examined for trait association and presence of polymorphism in breeding lines and populations. However, with recent advances in tomato sequencing, it is becoming increasingly possible to develop more informative markers to accelerate the use of MAS in tomato breeding.


Disease resistance Marker validation Molecular breeding Molecular markers Solanum lycopersicum 



We would like to thank Professors John Williamson, Bryon Sosinski and Allan Brown, Drs. Matthew Kinkade and Heather Merk, and graduate students Matthew Sullenberger, Erik Ohlson and Yang Bian for reviewing the manuscript before submission and helpful suggestions. Technical help of Ragy Ibrahem is highly appreciated.


  1. Agrios GN (2004) Plant pathology. Fifth edn. Elsevier, New YorkGoogle Scholar
  2. Ammiraju JSS, Veremis JC, Huang X, Roberts PA, Kaloshian I (2003) The heat-stable root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6. Theor Appl Genet 106:478–484PubMedGoogle Scholar
  3. Arens P, Mansilla C, Deinum D, Cavellini L, Moretti A, Rolland S, van der Schoot H, Calvache D, Ponz F, Collonnier C, Mathis R, Smilde D, Caranta C, Vosman B (2010) Development and evaluation of robust molecular markers linked to disease resistance in tomato for distinctness, uniformity and stability testing. Theor Appl Genet 120:655–664PubMedCrossRefGoogle Scholar
  4. Barillas AC, Mejia L, Sanchez-Perez A, Maxwwell DP (2008) CAPS and SCAR markers for detection of I-3 gene introgression for resistance to Fusarium oxysporium f.sp. lycopersici race 3. Rep Tomato Genet Coop 58:11–17Google Scholar
  5. Bernatzky R, Tanksley SD (1986) Towards a saturated linkage map in tomato based on isozymes and random cDNA sequences. Genetics 112:887–898PubMedGoogle Scholar
  6. Black LL, Wang TC, Hanson PM, Chen JT (1996) Late blight resistance in four wild tomato accessions: effectiveness in diverse locations and inheritance of resistance. Phytopathology 86:S24Google Scholar
  7. Chague V, Mercier JC, Guenard M, deCourcel A, Vedel F (1996) Identification and mapping on chromosome 9 of RAPD markers linked to Sw-5 in tomato by bulked segregant analysis. Theor Appl Genet 92:1045–1051CrossRefGoogle Scholar
  8. Chunwongse J, Chunwongse C, Black L, Hanson P (2002) Molecular mapping of the Ph-3 gene for late blight resistance in tomato. J Horticult Sci Biotechnol 77:281–286Google Scholar
  9. Cirulli M, Alexander LJ (1969) Influence of temperature and strain of tobacco mosaic virus on resistance in a tomato breeding line derived from Lycopersicon peruvianum. Phytopathology 59:1287–1297Google Scholar
  10. Danesh D, Aarons S, McGill GE, Young ND (1994) Genetic dissection of oligogenic resistance to bacterial wilt in tomato. Mol Plant-Microbe Interact 7:464–471PubMedCrossRefGoogle Scholar
  11. Dax E, Livneh O, Edelbaum O, Kedar N, Gavish N, Karchi H, Milo J, Sela I, Rabinowitch HD (1994) A random amplified polymorphic DNA (RAPD) molecular marker for the Tm-2a gene in tomato. Euphytica 74:159–163CrossRefGoogle Scholar
  12. Dax E, Livneh O, Aliskevicius E, Edelbaum O, Kedar N, Gavish N, Milo J, Geffen F, Blumenthal A, Rabinowich HD, Sela I (1998) A SCAR marker linked to the ToMV resistance gene, Tm2(2), in tomato. Euphytica 101:73–77CrossRefGoogle Scholar
  13. Devran Z, Sogut MA, Gozel U, Tor M, Elekcioglu IH (2008) Analysis of genetic variation between populations of Meloidogyne spp. from Turkey. Russ J Nematol 16:143–149Google Scholar
  14. Dianese EC, de Fonseca MEN, Goldbach R, Kormelink R, Inoue-Nagata AK, Resende RO, Boiteux LS (2010) Development of a locus-specific, co-dominant SCAR marker for assisted-selection of the Sw-5 (Tospovirus resistance) gene cluster in a wide range of tomato accessions. Mol Breed 25:133–142CrossRefGoogle Scholar
  15. El Mohtar CA, Atamian HS, Dagher RB, Abou-Jawdah Y, Salus MS, Maxwell DP (2007) Marker-assisted selection of tomato genotypes with the I-2 gene for resistance to Fusarium oxysporum f. sp lycopersici race 2. Plant Dis 91:758–762CrossRefGoogle Scholar
  16. FAOSTAT (2008) FAO Statistical Databases. Food and agriculture organization of the United Nations, Statistics Division. ( 2011
  17. Finlay KW (1953) Inheritance of spotted wilt resistance in tomatoes; five gene controllinng spotted wilt resistance in four tomatoes. Aust J Biol Sci 6:153–163PubMedGoogle Scholar
  18. Foolad M (2007) Genome mapping and molecular breeding of tomato. Int J Plant Genomics 2007:52. doi: 10.1155/2007/64358
  19. Foolad MR, Merk HL, Ashrafi H (2008) Genetics, genomics and breeding of late blight and early blight resistance in tomato. Crit Rev Plant Sci 27:75–107CrossRefGoogle Scholar
  20. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209CrossRefGoogle Scholar
  21. Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilizatioin of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467PubMedCrossRefGoogle Scholar
  22. Gardner RG, Panthee DR (2010) ‘Plum Regal’ fresh-market plum tomato hybrid and its parents, NC 25P and NC 30P. HortScience 45:824–825Google Scholar
  23. Garland S, Sharman M, Persley D, McGrath D (2005) The development of an improved PCR-based marker system for Sw-5, an important TSWV resistance gene of tomato. Aust J Agric Res 56:285–289. doi: 10.1071/ar04140 CrossRefGoogle Scholar
  24. Goodwin SB, Schneider RE, Fry WE (1995) Use of cellulose-acetate electrophoresis for rapid identification of allozyme genotypes of Phytophthora infestans. Plant Dis 79:1181–1185CrossRefGoogle Scholar
  25. Grimault V, Prior P, Anais G (1995) A monogenic dominant resistance of tomato to bacterial wilt in Hawaii-7996 is associated with plant colonization by Pseudomonas solanacearum. J Phytopathol 143:349–352CrossRefGoogle Scholar
  26. Hanson PM, Licardo O, Hanudin WangJ-F, Chen J-t (1998) Diallel analysis of bacterial wilt resistance in tomato derived from different sources. Plant Dis 82:74–78. doi: 10.1094/PDIS.1998.82.1.74 CrossRefGoogle Scholar
  27. Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2004) Fine mapping of the tomato I-3 gene for fusarium wilt resistance and elimination of a co-segregating resistance gene analogue as a candidate for I-3. Theor Appl Genet 109:409–418PubMedCrossRefGoogle Scholar
  28. Jablonska B, Ammiraju JSS, Bhattarai KK, Mantelin S, de Ilarduya OM, Roberts PA, Kaloshian I (2007) The Mi-9 gene from Solanum arcanum conferring heat-stable resistance to root-knot nematodes is a homolog of Mi-1. Plant Physiol 143:1044–1054PubMedCrossRefGoogle Scholar
  29. Kiewnick S, Dessimoz M, Franck L (2009) Effects of the Mi-1 and the N root-knot nematode-resistance gene on infection and reproduction of Meloidogyne enterolobii on tomato and pepper cultivars. J Nematol 41:134–139PubMedGoogle Scholar
  30. Lanfermeijer FC, Warmink J, Hille J (2005) The products of the broken Tm-2 and the durable Tm-2(2) resistance genes from tomato differ in four amino acids. J Exp Bot 56:2925–2933. doi: 10.1093/jxb/eri288 PubMedCrossRefGoogle Scholar
  31. Langella R, Ercolano MR, Monti LM, Frusciante L, Barone A (2004) Molecular marker assisted transfer of resistance to TSWV in tomato elite lines. J Hortic Sci Biotechnol 79:806–810Google Scholar
  32. Lim GTT, Wang GP, Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2006) Mapping the I-3 gene for resistance to Fusarium wilt in tomato: application of an I-3 marker in tomato improvement and progress towards the cloning of I-3. Australas Plant Pathol 35:671–680CrossRefGoogle Scholar
  33. Lim G, Wang GP, Hemming M, McGrath D, Jones D (2008) High resolution genetic and physical mapping of the I-3 region of tomato chromosome 7 reveals almost continuous microsynteny with grape chromosome 12 but interspersed microsynteny with duplications on Arabidopsis chromosomes 1, 2 and 3. Theor Appl Genet 118:57–75PubMedCrossRefGoogle Scholar
  34. Mangin B, Thoquet P, Olivier J, Grimsley NH (1999) Temporal and multiple quantitative trait loci analyses of resistance to bacterial wilt in tomato permit the resolution of linked loci. Genetics 151:1165–1172PubMedGoogle Scholar
  35. Medina-Filho H, Stevens M (1980) Tomato breeding for nematode resistance: survey of resistant varieties for horticultural characterisitcs and genotype of acid phosphatase. Acta Hort 100:383–391Google Scholar
  36. Mejía L, Garcia BE, Fulladolsa AC, Ewert ER, Wang JF, Scott JW, Allen C, Maxwell DP (2009) Evaluation of recombinant inbred lines for resistance to Ralstonia solanacearum in Guatemala and preliminary data on PCR-based tagging of introgressions associated with bacterial wilt-resistant line, Hawaii 7996. Rpt Tomato Genetic Coop 59:32–41Google Scholar
  37. Merk HL, Foolad MR (2011) Parent-offspring correlation estimate of heritability for late blight resistance conferred by an accession of the tomato wild species Solanum pimpinellifolium. Plant Breed (in press)Google Scholar
  38. Miao LX, Shou SY, Cai JY, Jiang F, Zhu ZJ, Li HB (2009) Identification of two AFLP markers linked to bacterial wilt resistance in tomato and conversion to SCAR markers. Mol Biol Rep 36:479–486. doi: 10.1007/s11033-007-9204-1 PubMedCrossRefGoogle Scholar
  39. Moon H, Nicholson JS (2007) AFLP and SCAR markers linked to tomato spotted wilt virus resistance in tobacco. Crop Sci 47:1887–1894CrossRefGoogle Scholar
  40. Moreau P, Thoquet P, Olivier J, Laterrot H, Grimsley N (1998) Genetic mapping of Ph-2, a single locus controlling partial resistance to Phytophthora infestans in tomato. Mol Plant-Microbe Interact 11:259–269CrossRefGoogle Scholar
  41. Mutlu N, Boyaci FH, Gocmen M, Abak K (2008) Development of SRAP, SRAP-RGA, RAPD and SCAR markers linked with a Fusarium wilt resistance gene in eggplant. Theor Appl Genet 117:1303–1312PubMedCrossRefGoogle Scholar
  42. Ohmori T, Murata M, Motoyoshi F (1996) Molecular characterization of RAPD and SCAR markers linked to the Tm-1 locus in tomato. Theor Appl Genet 92:151–156CrossRefGoogle Scholar
  43. Ori N, Eshed Y, Paran I, Presting G, Aviv D, Tanksley S, Zamir D, Fluhr R (1997) The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9:521–532PubMedGoogle Scholar
  44. Panthee DR, Gardner RG (2010) ‘Mountain Merit’: a late blight-resistant large-fruited tomato hybrid. HortScience 45:1547–1548Google Scholar
  45. Peirce LC (1971) Linkage tests with Ph conditioning resistance to race 0, Phytophthora infestans. Rep Tomato Genet Coop 21:30Google Scholar
  46. Pillen K, Pineda O, Lewis C, Tanksley SD (1996) Status of genome mapping tools in the taxon Solanaceae. In: Paterson A (ed) Genome mapping in plants. RG Landes Austin, Texas, pp 281–308Google Scholar
  47. Robbins MD, Masud MAT, Panthee DR, Gardner CO, Francis D, Stevens MA (2010) Marker-assisted selection for coupling phase resistance to tomato spotted wilt virus and Phytophthora infestans (late blight) in tomato. HortScience 45:1424–1428Google Scholar
  48. Rosello S, Ricarte B, Diez MJ, Nuez F (2001) Resistance to tomato spotted wilt virus introgressed from Lycopersicon peruvianum in line UPV 1 may be allelic to Sw-5 and can be used to enhance the resistance of hybrids cultivars. Euphytica 119:357–367CrossRefGoogle Scholar
  49. Saidi M, Warade SD (2008) Tomato breeding for resistance to tomato spotted wilt virus (TSWV): An overview of conventional and molecular approaches. Czech J Genet Plant Breed 44:83–92Google Scholar
  50. Scott J (2007) Breeding for resistance to viral pathogens. In: Razdan MK, Matton AK (eds) Genetic improvement of solanaceous crops. Vol 2. Tomato. Science Publishers, Enfield, pp 457–485Google Scholar
  51. Scott JW (2008) Fresh market tomato breeding in the USA. Acta Hort 789:21–25Google Scholar
  52. Scott JW, Somodi GC, Jones JB (1988) Bacterial spot resistance is not associated with bacterial wilt resistance in tomato. Proc Fla State Hort Soc 101:390–392Google Scholar
  53. Scott JW, Agrama HA, Jones JP (2004) RFLP-based analysis of recombination among resistance genes to Fusarium wilt races 1, 2, and 3 in tomato. J Am Soc Hort Sci 129:394–400Google Scholar
  54. Scott JW, Wang JF, Hanson PM (2005) Breeding tomatoes for resistance to bacterial wilt, a global view. Proc 1st Intl Symp Tomato Dis 695:161–172Google Scholar
  55. Seah S, Williamson VM, Garcia BE, Mejía L, Salus MS, Martin CT, Maxwell DP (2007) Evaluation of a co-dominant SCAR marker for detection of the Mi-1 locus for resistance to root-knot nematode in tomato germplasm. Rep Tomato Genet Coop 57:37–40Google Scholar
  56. Sela-Buurlage MB, Budai-Hadrian O, Pan Q, Carmel-Goren L, Vunsch R, Zamir D, Fluhr R (2001) Genome-wide dissection of Fusarium resistance in tomato reveals multiple complex loci. Mol Genet Genomics 265:1104–1111PubMedCrossRefGoogle Scholar
  57. Smiech M, Rusinowski Z, Malepszy S, Niemirowicz-Szczytt K (2000) New RAPD markers of tomato spotted wilt virus (TSWV) resistance in Lycopersicon esculentum Mill. Acta Physiol Plant 22:299–303CrossRefGoogle Scholar
  58. Sobir OhmoriT, Murata M, Motoyoshi F (2000) Molecular characterization of the SCAR markers tightly linked to the Tm-2 locus of the genus Lycopersicon. Theor Appl Genet 101:64–69CrossRefGoogle Scholar
  59. Stevens MR, Scott SJ, Gergerich RC (1992) Inheritance of gene for resistance to tomato spotted wilt virus (TSWV) from Lycopersicon Peruvianum Mill. Euphytica 59:9–17Google Scholar
  60. Stevens MR, Lamb EM, Rhoads DD (1995) Mapping the Sw-5 locus for tomato spotted wilt virus resistance in tomatoes using RAPD and RFLP analysis. Theor Appl Genet 90:451–456CrossRefGoogle Scholar
  61. Tanksley SD (1983) Molecular markers in plant breeding. Plant Mol Biol Rep 1:3–8CrossRefGoogle Scholar
  62. Tanksley SD, Ganal MW, Prince JP, Devicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High-density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160PubMedGoogle Scholar
  63. Thoquet P, Olivier J, Sperisen C, Rogowsky P, Prior P, Anais G, Mangin B, Bazin B, Nazer R, Grimsley N (1996) Polygenic resistance of tomato plants to bacterial wilt in the French West Indies. Mol Plant-Microbe Interact 9:837–842CrossRefGoogle Scholar
  64. USDA-NASS (2008) Agricultural statistics. United State Department of Agtriculture, National Agricultural Staticstics Service (
  65. Wang JF, Olivier J, Thoquet P, Mangin B, Sauviac L, Grimsley NH (2000) Resistance of tomato line Hawaii 7996 to Ralstonia solanacearum Pss4 in Taiwan is controlled mainly by a major strain-specific locus. Mol Plant-Microbe Interact 13:6–13PubMedCrossRefGoogle Scholar
  66. Williamson VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36:277–293PubMedCrossRefGoogle Scholar
  67. Williamson VM, Ho JY, Wu FF, Miller N, Kaloshian I (1994) A PCR-based marker tightly linked to the nematode resistance gene, Mi, in tomato. Theor Appl Genet 87:757–763CrossRefGoogle Scholar
  68. Yaghoobi J, Yates JL, Williamson VM (2005) Fine mapping of the nematode resistance gene Mi-3 in Solanum peruvianum and construction of a S. lycopersicum DNA contig spanning the locus. Mol Genet Genomics 274:60–69PubMedCrossRefGoogle Scholar
  69. Yang W, Francis DM (2007) Genetics and breeding for resistance to bacterial diseases in tomato: prospects for marker-assisted selection. In: Razdan MK, Matton AK (eds) Genetic improvement of solanaceous crops. Vol 2. Tomato. Science Publishers, Enfield, pp 379–419Google Scholar
  70. Young ND, Zamir D, Ganal MW, Tanksley SD (1988) Use of isogenic lines and simultaneous probing to identify DNA markers tightly linked to the Tm-2 alpha gene in tomato. Genetics 120:579–585PubMedGoogle Scholar
  71. Zaccardelli M, Perrone D, Del Galdo A, Campanile F, Parrella G, Giordano I (2008) Tomato genotypes resistant to tomato spotted wilt virus evaluated in open field crops in southern Italy. Acta Hort 789:147–150Google Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Horticultural ScienceNorth Carolina State University, Mountain Horticultural Crops Research and Extension CenterMills RiverUSA
  2. 2.Department of Horticulture and The Intercollege Graduate Degree Programs in Plant Biology and GeneticsThe Pennsylvania State UniversityUniversity ParkUSA

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