Plant Molecular Biology Reporter

, Volume 31, Issue 2, pp 352–362 | Cite as

Mapping of a Heat-Stable Gene for Resistance to Southern Root-Knot Nematode in Solanum lycopersicum

  • Yinlei Wang
  • Wencai Yang
  • Wei Zhang
  • Qing Han
  • Miao Feng
  • Huolin Shen
Original Paper


Root-knot nematodes (Meloidogyne spp.) can cause severe problems in tomato production in warm climates. To date, Mi-1 is the only gene that has been used widely to develop cultivars for controlling disease caused by nematodes around the world. However, Mi-1 does not provide resistance to the pest when the soil temperature is above 28 °C. Tomato breeding line ZN17 has been reported to possess resistance to Meloidogyne incognita at high temperatures (32 °C). To identify markers linked tightly to resistance, an F2 population was developed by crossing the resistance line ZN17 to susceptible line 09C84. Analysis of F2 individuals by inoculating M. incognita suggested that resistance in ZN17 is conditioned by a single dominant gene temporarily designated as Mi-HT. Linkage analysis suggested that Mi-HT is located on the short arm of chromosome 6. One marker, W737, co-segregated with Mi-HT. Comparisons of map positions of Mi-HT, Mi-1, and Mi-9, as well as marker genotypes in LA2157, Motelle, and ZN17 suggested that Mi-HT might be a homologue of Mi-1 and Mi-9 or a new gene. The results obtained in this study will facilitate fine-mapping and cloning of the gene as well as marker-assisted breeding for heat-stable resistance to southern root-knot nematodes in tomato.


Tomato Heat-stable resistance Root-knot nematode Mapping 



The work was supported by Chinese National Key Project (2009ZX08009-064B).


  1. Ammati M, Thomason I, McKinney H (1986) Retention of resistance to Meloidogyne incognita in Lycopersicon genotypes at high soil temperature. J Nematol 18:491–495PubMedGoogle Scholar
  2. Ammiraju JS, 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. Carter WW (1982) Influence of soil temperature on Meloidogyne incognita resistant and susceptible cotton, Gossypium hirsutum. J Nematol 14:343–346PubMedGoogle Scholar
  4. Castagnone-Sereno P, Wajnberg E, Bongiovanni M, Leroy F, Dalmasso A (1994) Genetic variation in Meloidogyne incognita virulence against the tomato Mi resistance gene: evidence from isofemale line selection studies. Theor Appl Genet 88:749–753CrossRefGoogle Scholar
  5. Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C (2001) New data on the specificity of the root-knot nematode resistance genes Mel and Me3 in pepper. Plant Breed 120:429–433CrossRefGoogle Scholar
  6. Chen J, Wang H, Shen H, Chai M, Li J, Qi M, Yang W (2009) Genetic variation in tomato populations from four breeding programs revealed by single nucleotide polymorphism and simple sequence repeat markers. Sci Hortic 122:6–16CrossRefGoogle Scholar
  7. Cota-Sanchez JH, Remarchuk K, Ubayasena K (2006) Ready-to-use DNA extracted with a CTAB method adapted for herbarium specimens and mucilaginous plant tissue. Plant Mol Biol Rep 24:161–167CrossRefGoogle Scholar
  8. Czembor PC, Arseniuk E, Czaplicki A, Song Q, Cregan PB, Ueng PP (2003) QTL mapping of partial resistance in winter wheat to Stagonospora nodorum blotch. Genome 46:546–554PubMedCrossRefGoogle Scholar
  9. de Jong CF, Takken FLW, Cai XH, de Wit P, Joosten M (2002) Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Mol Plant Microbe Interact 15:1040–1049PubMedCrossRefGoogle Scholar
  10. Dixon MS, Jones DA, Hatzixanthis K, Ganal MW, Tanksley SD, Jones JDG (1995) High-resolution mapping of the physical location of the tomato Cf-2 gene. Mol Plant Microbe Interact 8:200–206PubMedCrossRefGoogle Scholar
  11. Doganlar S, Frary A, Tanksley SD (1997) Production of interspecific F-1 hybrids, BC1, BC2 and BC3 populations between Lycopersicon esculentum and two accessions of Lycopersicon peruvianum carrying new root-knot nematode resistance genes. Euphytica 95:203–207CrossRefGoogle Scholar
  12. Dropkin VH (1969) The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59:1632–1637Google Scholar
  13. Griffin GD (1969) Effects of temperature on Meloidogyne hapla in alfalfa. Phytopathology 59:599–602Google Scholar
  14. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312PubMedCrossRefGoogle Scholar
  15. Jablonska B, Ammiraju JSS, Bhattarai KK, Mantelin S, Martinez de Ilarduya O, 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
  16. Jatala P, Russell CC (1972) Nature of sweet potato resistance to Meloidogyne incognita and the effects of temperature on parasitism. J Nematol 4:1–7PubMedGoogle Scholar
  17. Kabelka E, Franchino B, Francis DM (2002) Two loci from Lycopersicon hirsutum LA407 confer resistance to strains of Clavibacter michiganensis subsp michiganensis. Phytopathology 92:504–510PubMedCrossRefGoogle Scholar
  18. Kaloshian I, Williamson VM, Miyao G, Lawn DA, Westerdahl BB (1996) “Resistance-breaking” nematodes identified in California tomatoes. Calif Agric 50:18–19CrossRefGoogle Scholar
  19. Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P, Zabel P, Williamson VM (1998) Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol Gen Genet 257:376–385PubMedCrossRefGoogle Scholar
  20. Lamberti F (1979) Economic importance of Meloidogyne spp. in subtropical and Mediterranean climates. In: Lamberti F, Taylor CE (eds) Root-knot nematodes (Meloidogyne spp.): Systematic, biology and control. Academic, New York, pp 342–357Google Scholar
  21. Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832PubMedCrossRefGoogle Scholar
  22. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root-knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319PubMedGoogle Scholar
  23. Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant Microbe Interact 16:645–649PubMedCrossRefGoogle Scholar
  24. Pegard A, Brizzard G, Fazari A, Soucaze O, Abad P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology 95:158–165PubMedCrossRefGoogle Scholar
  25. Roberts P, Dalmasso A, Cap GB, Castagnone-Sereno P (1990) Resistance in Lycopersicon peruvianum to isolates of Mi gene-compatible Meloidogyne populations. J Nematol 22:585PubMedGoogle Scholar
  26. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754PubMedCrossRefGoogle Scholar
  27. Sasser J (1977) Worldwide dissemination and importance of the root-knot nematodes, Meloidogyne spp. J Nematol 9:26–29PubMedGoogle Scholar
  28. Seah S, Yaghoobi J, Rossi M, Gleason CA, Williamson VM (2004) The nematode-resistance gene, Mi-1, is associated with an inverted chromosomal segment in susceptible compared to resistant tomato. Theor Appl Genet 108:1635–1642PubMedCrossRefGoogle Scholar
  29. Smith PG (1944) Embryo culture of a tomato species hybrid. Proc Am Soc Hortic Sci 44:413–416Google Scholar
  30. Tang X, Szinay D, Lang C, Ramanna MS, van der Vossen EA, Datema E, Lankhorst RK, de Boer J, Peters SA, Bachem C, Stiekema W, Visser RG, de Jong H, Bai Y (2008) Cross-species bacterial artificial chromosome-fluorescence in situ hybridization painting of the tomato and potato chromosome 6 reveals undescribed chromosomal rearrangements. Genetics 180:1319–1328PubMedCrossRefGoogle Scholar
  31. Tzortzakakis EA, Adam MAM, Blok VC, Paraskevopoulos C, Bourtzis K (2005) Occurrence of resistance-breaking populations of root-knot nematodes on tomato in Greece. Eur J Plant Pathol 113:101–105CrossRefGoogle Scholar
  32. Van Ooijen J, Voorrips R (2001) JoinMap v. 3, software in the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  33. Verlaan MG, Szinay D, Hutton SF, de Jong H, Kormelink R, Visser RG, Scott JW, Bai Y (2011) Chromosomal rearrangements between tomato and Solanum chilense hamper mapping and breeding of the TYLCV resistance gene Ty-1. Plant J 68:1093–1103PubMedCrossRefGoogle Scholar
  34. Whitham S, McCormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Natl Acad Sci USA 93:8776–8781PubMedCrossRefGoogle Scholar
  35. Williamson VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36:277–293PubMedCrossRefGoogle Scholar
  36. 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
  37. Wu WW, Shen HL, Yang WC (2009) Sources for heat-stable resistance to southern root-knot nematode (Meloidogyne incognita) in Solanum lycopersicum. Agric Sci China 8:697–702CrossRefGoogle Scholar
  38. Xiao SY, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15:33–45PubMedCrossRefGoogle Scholar
  39. 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
  40. Yang W, Bai X, Kabelka E, Eaton C, Kamoun S, van der Knaap E, Francis D (2004) Discovery of single nucleotide polymorphisms in Lycopersicon esculentum by computer aided analysis of expressed sequence tags. Mol Breeding 14:21–34CrossRefGoogle Scholar
  41. Zhang LY, Zhang YY, Chen RG, Zhang JH, Wang TT, Li HX, Ye ZB (2010) Ectopic expression of the tomato Mi-1 gene confers resistance to root knot nematodes in lettuce (Lactuca sativa). Plant Mol Biol Rep 28:204–211CrossRefGoogle Scholar
  42. Zhou B, Dolan M, Sakai H, Wang GL (2007) The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. Mol Plant Microbe Interact 20:63–71PubMedCrossRefGoogle Scholar
  43. Zhou G, Ye Q, Wang R (2010) Hybrids resistant to root-knot nematodes of tomato obtained by embryo-rescuing and molecular marker-assisted selection. J Zhejiang Univ (Agric Life Sci) 36:255–261Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Yinlei Wang
    • 1
  • Wencai Yang
    • 1
  • Wei Zhang
    • 1
  • Qing Han
    • 1
  • Miao Feng
    • 1
  • Huolin Shen
    • 1
  1. 1.Department of Vegetable ScienceChina Agricultural UniversityBeijingChina

Personalised recommendations