Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Research Article
  • Published:

The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids

Nature Biotechnology volume 16, pages 1365–1369 (1998)Cite this article

Abstract

Mi-1, a Lycopersicon peruvianum gene conferring resistance to the agricultural pests, root-knot nematodes, and introgressed into tomato, has been cloned using a selective restriction fragment amplification based strategy. Complementation analysis of a susceptible tomato line with a 100 kb cosmid array yielded a single cosmid clone capable of conferring resistance both to the root-knot nematode Meloidogyne incognita and to an unrelated pathogen, the potato aphid Macrosiphum euphorbiae. This resistance was stable. The Mi-1 gene encodes a protein sharing structural features with the nucleotide-binding site leucine-rich repeat–containing type of plant resistance genes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Positional cloning of Mi-1.
Figure 2: Root-knot nematode (Meloidogyne incognita) resistance. (A) The root system of a susceptible control plant (52201).
Figure 3: Potato aphid (Macrosiphum euphorbiae) resistance.
Figure 4: Structure of the Mi-1 gene.
Figure 5: Identification of Mi-1 homologs.

Similar content being viewed by others

References

  1. Mai, W.F. 1985. Plant-parasitic nematodes: their threat to agriculture, pp 11–17 in Advanced treatise on meloidogyne, Vol. I. Sasser, J.N. and Carter, C.C. (eds.), North Carolina State University Graphics, Raleigh, NC.

    Google Scholar 

  2. Bailey, D.M. 1941. The seedling test method for root-knot nematode resistance. Proc. Am. So. Hortic. Sci. 38: 573–575.

    Google Scholar 

  3. Gilbert, J.C. and McGuire, D.C. 1956. Inheritance of resistance to several root-knot from Meloidogyne incognita in commercial type tomatoes. Proc. Am. So. Hortic. Sci. 68: 437–442.

    Google Scholar 

  4. Kaloshian, I., Harry Lange, W., and Williamson, V. 1995. An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc. Natl. Acad. Sci. USA 92: 622– 625.

    Article  Google Scholar 

  5. Blackman, R.L. and Eastop, V.F. 1984. Aphids on the world's crops: an identification and information guide. John Wiley & Sons, New York.

    Google Scholar 

  6. Baker, B., Zambryski, P., Staskawicz, B., and Dinesh-Kumar, S.P. 1997. Signaling in plant-microbe interactions. Science 276: 726–733.

    Article  Google Scholar 

  7. Hammond-Kosack, K.E. and Jones, J.D.G. 1997 . Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 573–607.

    Article  Google Scholar 

  8. De Wit, P.J.G.M. 1997. Pathogen avirulence and plant resistance: a key role for recognition. Trends in Plant Science 2: 452–458.

    Article  Google Scholar 

  9. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M. et al. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407– 4414.

    Article  Google Scholar 

  10. Simons, G., Van der Lee, T., Diergaarde, P., Van Daelen, R., Groenendijk, J., Frijters, A. et al. 1997. AFLP-based fine mapping of the Mlo gene to a 30-kb DNA segment of the barley genome. Genomics 44: 61–70.

    Article  Google Scholar 

  11. Kaloshian, I., Yaghoobi, J., Liharska, T.B., Hontelez, J., Hanson, D., Hogan, P. et al. 1998. Genetic and physical localization of the root-knot nematode resistance locus Mi in tomato. Mol. Gen. Genet. 257: 376–385.

    Article  Google Scholar 

  12. Bairoch, A., Bucher, P., and Hofmann, K, 1997. The PROSITE database, its status in 1997. Nucleic Acids Res. 25: 217 –221.

    Article  Google Scholar 

  13. Hofmann, K. and Bucher, P. 1998. The PCI domain: a common theme in three multiprotein complexes. TIBS 23: 204–205.

    Google Scholar 

  14. Salmeron, J.M., Oldroyd, G.E.D., Rommens, C.M.T., Scofield, S.R., Kim, H-S., Lavelle, D.T. et al. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86: 123–133.

    Article  Google Scholar 

  15. Jones, D.A. and Jones, J.D.G. 1997. The role of leucine-rich repeat proteins in plant defenses. Adv. Bot. Res. 24: 89–167.

    Article  Google Scholar 

  16. Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A. et al. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843– 846.

    Article  Google Scholar 

  17. Yaghoobi, J., Kaloshian, I., Wen, Y., and Williamson, V.M. 1995. Mapping a new nematode resistance locus in Lycopersicon peruvianum. Theor. Appl. Genet. 91: 457 –464.

    Article  Google Scholar 

  18. Veremis, J.C. and Roberts, P.A. 1996. Relationships between Meloidogyne incognita resistance genes in Lycopersicon peruvianum differentiated by heat sensitivity and nematode virulence. Theor. Appl. Genet. 93: 950–959.

    Article  Google Scholar 

  19. Dickinson, M.J., Jones, D.A., and Jones, J.D.G. 1993. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol. Plant. Microbe Interact. 6: 341–347.

    Article  Google Scholar 

  20. Rouppe van der Voort, J., Wolters, P., Folkertsma, R., Hutten, R., Van Zandvoort P., Vinke H. et al. 1997. Mapping of the cyst nematode resistance locus Gpa2 in potato using a strategy based on comigrating AFLP markers. Theor. Appl. Genet. 95: In press.

  21. Cai, D., Kleine, M., Kilfe, S., Harloff, H-J., Sandral, N.N., Marcker, K.A. et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275: 832– 835.

    Article  Google Scholar 

  22. Bisgrove, S., Simonich, M., Smith, N., Sattler, N., and Innes, R. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927–933.

    Article  Google Scholar 

  23. Hammond-Kosack, K.E., Tang, S., Harrison, K., and Jones, J.D.G. 1998 . The tomato Cf-9 resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr9. Plant Cell 10: 1251–1258 .

    Google Scholar 

  24. Jones J.D.G., Shlumukov, L., Carland, F., English, J., Scofield, S.R., Bishop, G.J. et al. 1992. Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res. 1: 285–297.

    Article  Google Scholar 

  25. Simons, G., Groenendijk, J., Wijbrandi, J., Reijans, M., Groenen, J., Diergaarde, P. et al. 1998. Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10: 1055– 1068.

    Article  Google Scholar 

  26. Lazo, G.R., Stein, P.A., and Ludwig, R.A. 1991. A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Bio/Technology 9: 963–971.

    Article  Google Scholar 

  27. Deblaere, R., Reynaerts, A., Höfte, H., Hernalsteens, J.P., Leemans, J., and Van Montagu, M. 1987. Vectors for cloning in plant cells. Methods. Enzymol. 153: 277– 292.

    Article  Google Scholar 

  28. Koornneef, M., Jongsma, M. Weide, R., Zabel, P., and Hille, J. 1987. Transformation of tomato, pp. 169– 178, in Tomato biotechnology. Nevins, D.J. and Jones, R.A. (eds.) Alan R. Liss, New York.

    Google Scholar 

  29. Dear, S. and Staden, R. 1991. A sequence assembly and editing program for efficient management of large projects. Nucleic Acids Res. 14: 3907–3911.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Jerina Pot and Maarten van Riel for artwork. We acknowledge the staff of De Ruiter Seeds and Enza Zaden for performing the nematode tests and of Rijk Zwaan for the aphid tests. This work was financed by Keygene N.V. and three Dutch breeding companies: De Ruiter Seeds, Enza Zaden, and Rijk Zwaan. Furthermore, this work was subsidized by the Dutch Ministry of Economic Affairs through a Programmatische Bedrijfsgerichte Technologie Stimulering grant. AFLP is a registered trademark of Keygene N.V.

Author information

Author notes

  1. Marc Zabeau§

    Present address: Helix, Onafhankelijkheidslaan 38, 9000, Gent, Belgium

  2. Tsvetana Liharska‡

    Present address: Department of Genetics, Free University of Amsterdam, De Boelelaan 1087, 1081 HV, Amsterdam, The Netherlands

  3. Pieter Vos and Guus Simons: These authors contributed equally to this work.

Authors and Affiliations

  1. Keygene N.V., Agro Business Park, P.O. Box 216, 6700 AE, Wageningen, The Netherlands

    Pieter Vos†, Guus Simons†, Taco Jesse, Jelle Wijbrandi, Leo Heinen, René Hogers, Adri Frijters, John Groenendijk, Paul Diergaarde, Martin Reijans, Joke Fierens-Onstenk, Michiel de Both, Johan Peleman & Marc Zabeau§

  2. Department of Molecular Biology, Wageningen Agricultural University, Dreyenlaan 3, 6709 DB, Wageningen, The Netherlands

    Tsvetana Liharska‡ & Jan Hontelez

Authors
  1. Pieter Vos†
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guus Simons†
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taco Jesse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jelle Wijbrandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leo Heinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. René Hogers
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Adri Frijters
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John Groenendijk
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Paul Diergaarde
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Martin Reijans
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Joke Fierens-Onstenk
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Michiel de Both
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Johan Peleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Tsvetana Liharska‡
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jan Hontelez
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Marc Zabeau§
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pieter Vos†.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vos†, P., Simons†, G., Jesse, T. et al. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16, 1365–1369 (1998). https://doi.org/10.1038/4350

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/4350

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing