Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1998 Aug;10(8):1307–1319. doi: 10.1105/tpc.10.8.1307

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.

S B Milligan 1, J Bodeau 1, J Yaghoobi 1, I Kaloshian 1, P Zabel 1, V M Williamson 1
PMCID: PMC144378  PMID: 9707531

Abstract

The Mi locus of tomato confers resistance to root knot nematodes. Tomato DNA spanning the locus was isolated as bacterial artificial chromosome clones, and 52 kb of contiguous DNA was sequenced. Three open reading frames were identified with similarity to cloned plant disease resistance genes. Two of them, Mi-1.1 and Mi-1.2, appear to be intact genes; the third is a pseudogene. A 4-kb mRNA hybridizing with these genes is present in tomato roots. Complementation studies using cloned copies of Mi-1.1 and Mi-1.2 indicated that Mi-1.2, but not Mi-1.1, is sufficient to confer resistance to a susceptible tomato line with the progeny of transformants segregating for resistance. The cloned gene most similar to Mi-1.2 is Prf, a tomato gene required for resistance to Pseudomonas syringae. Prf and Mi-1.2 share several structural motifs, including a nucleotide binding site and a leucine-rich repeat region, that are characteristic of a family of plant proteins, including several that are required for resistance against viruses, bacteria, fungi, and now, nematodes.

Full Text

The Full Text of this article is available as a PDF (339.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agulnik A. I., Mitchell M. J., Lerner J. L., Woods D. R., Bishop C. E. A mouse Y chromosome gene encoded by a region essential for spermatogenesis and expression of male-specific minor histocompatibility antigens. Hum Mol Genet. 1994 Jun;3(6):873–878. doi: 10.1093/hmg/3.6.873. [DOI] [PubMed] [Google Scholar]
  2. Bent A. F., Kunkel B. N., Dahlbeck D., Brown K. L., Schmidt R., Giraudat J., Leung J., Staskawicz B. J. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science. 1994 Sep 23;265(5180):1856–1860. doi: 10.1126/science.8091210. [DOI] [PubMed] [Google Scholar]
  3. Bent A. F. Plant Disease Resistance Genes: Function Meets Structure. Plant Cell. 1996 Oct;8(10):1757–1771. doi: 10.1105/tpc.8.10.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cai D., Kleine M., Kifle S., Harloff H. J., Sandal N. N., Marcker K. A., Klein-Lankhorst R. M., Salentijn E. M., Lange W., Stiekema W. J. Positional cloning of a gene for nematode resistance in sugar beet. Science. 1997 Feb 7;275(5301):832–834. doi: 10.1126/science.275.5301.832. [DOI] [PubMed] [Google Scholar]
  5. Calvi B. R., Hong T. J., Findley S. D., Gelbart W. M. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell. 1991 Aug 9;66(3):465–471. doi: 10.1016/0092-8674(81)90010-6. [DOI] [PubMed] [Google Scholar]
  6. Dangl J., Holub E. La dolce vita: a molecular feast in plant-pathogen interactions. Cell. 1997 Oct 3;91(1):17–24. doi: 10.1016/s0092-8674(01)80005-2. [DOI] [PubMed] [Google Scholar]
  7. Dixon M. S., Jones D. A., Keddie J. S., Thomas C. M., Harrison K., Jones J. D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. doi: 10.1016/s0092-8674(00)81290-8. [DOI] [PubMed] [Google Scholar]
  8. Ellis J., Lawrence G., Ayliffe M., Anderson P., Collins N., Finnegan J., Frost D., Luck J., Pryor T. Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu Rev Phytopathol. 1997;35:271–291. doi: 10.1146/annurev.phyto.35.1.271. [DOI] [PubMed] [Google Scholar]
  9. Fattaey A. R., Helin K., Dembski M. S., Dyson N., Harlow E., Vuocolo G. A., Hanobik M. G., Haskell K. M., Oliff A., Defeo-Jones D. Characterization of the retinoblastoma binding proteins RBP1 and RBP2. Oncogene. 1993 Nov;8(11):3149–3156. [PubMed] [Google Scholar]
  10. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldsbrough A., Belzile F., Yoder J. I. Complementation of the Tomato anthocyanin without (aw) Mutant Using the Dihydroflavonol 4-Reductase Gene. Plant Physiol. 1994 Jun;105(2):491–496. doi: 10.1104/pp.105.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
  13. Hammond-Kosack K. E., Jones J. D. Resistance gene-dependent plant defense responses. Plant Cell. 1996 Oct;8(10):1773–1791. doi: 10.1105/tpc.8.10.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hammond-Kosack Kim E., Jones Jonathan D. G. PLANT DISEASE RESISTANCE GENES. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):575–607. doi: 10.1146/annurev.arplant.48.1.575. [DOI] [PubMed] [Google Scholar]
  15. Ho J. Y., Weide R., Ma H. M., van Wordragen M. F., Lambert K. N., Koornneef M., Zabel P., Williamson V. M. The root-knot nematode resistance gene (Mi) in tomato: construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. Plant J. 1992 Nov;2(6):971–982. [PubMed] [Google Scholar]
  16. Hollingshead S., Vapnek D. Nucleotide sequence analysis of a gene encoding a streptomycin/spectinomycin adenylyltransferase. Plasmid. 1985 Jan;13(1):17–30. doi: 10.1016/0147-619x(85)90052-6. [DOI] [PubMed] [Google Scholar]
  17. Kaloshian I., Lange W. H., Williamson V. M. An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):622–625. doi: 10.1073/pnas.92.2.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaloshian I., Yaghoobi J., Liharska T., Hontelez J., Hanson D., Hogan P., Jesse T., Wijbrandi J., Simons G., Vos P. Genetic and physical localization of the root-knot nematode resistance locus mi in tomato. Mol Gen Genet. 1998 Feb;257(3):376–385. doi: 10.1007/s004380050660. [DOI] [PubMed] [Google Scholar]
  19. Keen N. T. Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet. 1990;24:447–463. doi: 10.1146/annurev.ge.24.120190.002311. [DOI] [PubMed] [Google Scholar]
  20. Kobe B., Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature. 1995 Mar 9;374(6518):183–186. doi: 10.1038/374183a0. [DOI] [PubMed] [Google Scholar]
  21. Lagudah E. S., Moullet O., Appels R. Map-based cloning of a gene sequence encoding a nucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome. 1997 Oct;40(5):659–665. doi: 10.1139/g97-087. [DOI] [PubMed] [Google Scholar]
  22. Lawrence G. J., Finnegan E. J., Ayliffe M. A., Ellis J. G. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell. 1995 Aug;7(8):1195–1206. doi: 10.1105/tpc.7.8.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Leister D., Ballvora A., Salamini F., Gebhardt C. A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet. 1996 Dec;14(4):421–429. doi: 10.1038/ng1296-421. [DOI] [PubMed] [Google Scholar]
  24. Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
  25. McBride K. E., Summerfelt K. R. Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Mol Biol. 1990 Feb;14(2):269–276. doi: 10.1007/BF00018567. [DOI] [PubMed] [Google Scholar]
  26. Mindrinos M., Katagiri F., Yu G. L., Ausubel F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 1994 Sep 23;78(6):1089–1099. doi: 10.1016/0092-8674(94)90282-8. [DOI] [PubMed] [Google Scholar]
  27. Newman T., de Bruijn F. J., Green P., Keegstra K., Kende H., McIntosh L., Ohlrogge J., Raikhel N., Somerville S., Thomashow M. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 1994 Dec;106(4):1241–1255. doi: 10.1104/pp.106.4.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ori N., Eshed Y., Paran I., Presting G., Aviv D., Tanksley S., Zamir D., Fluhr R. 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. 1997 Apr;9(4):521–532. doi: 10.1105/tpc.9.4.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Parker J. E., Coleman M. J. Molecular intimacy between proteins specifying plant-pathogen recognition. Trends Biochem Sci. 1997 Aug;22(8):291–296. doi: 10.1016/s0968-0004(97)01089-x. [DOI] [PubMed] [Google Scholar]
  30. Parker J. E., Coleman M. J., Szabò V., Frost L. N., Schmidt R., van der Biezen E. A., Moores T., Dean C., Daniels M. J., Jones J. D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell. 1997 Jun;9(6):879–894. doi: 10.1105/tpc.9.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rochester D. E., Winer J. A., Shah D. M. The structure and expression of maize genes encoding the major heat shock protein, hsp70. EMBO J. 1986 Mar;5(3):451–458. doi: 10.1002/j.1460-2075.1986.tb04233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rose G. E., Howard D. J., Watts M. R. Periorbital necrotising fasciitis. Eye (Lond) 1991;5(Pt 6):736–740. doi: 10.1038/eye.1991.135. [DOI] [PubMed] [Google Scholar]
  33. Salmeron J. M., Oldroyd G. E., Rommens C. M., Scofield S. R., Kim H. S., Lavelle D. T., Dahlbeck D., Staskawicz B. J. 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. 1996 Jul 12;86(1):123–133. doi: 10.1016/s0092-8674(00)80083-5. [DOI] [PubMed] [Google Scholar]
  34. Schwartz D. C., Cantor C. R. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell. 1984 May;37(1):67–75. doi: 10.1016/0092-8674(84)90301-5. [DOI] [PubMed] [Google Scholar]
  35. Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ. Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato. Science. 1996 Dec 20;274(5295):2063–2065. doi: 10.1126/science.274.5295.2063. [DOI] [PubMed] [Google Scholar]
  36. Shizuya H., Birren B., Kim U. J., Mancino V., Slepak T., Tachiiri Y., Simon M. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8794–8797. doi: 10.1073/pnas.89.18.8794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Song W. Y., Wang G. L., Chen L. L., Kim H. S., Pi L. Y., Holsten T., Gardner J., Wang B., Zhai W. X., Zhu L. H. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995 Dec 15;270(5243):1804–1806. doi: 10.1126/science.270.5243.1804. [DOI] [PubMed] [Google Scholar]
  38. Stemmer W. P. A 20-minute ethidium bromide/high-salt extraction protocol for plasmid DNA. Biotechniques. 1991 Jun;10(6):726–726. [PubMed] [Google Scholar]
  39. Takeuchi T., Yamazaki Y., Katoh-Fukui Y., Tsuchiya R., Kondo S., Motoyama J., Higashinakagawa T. Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev. 1995 May 15;9(10):1211–1222. doi: 10.1101/gad.9.10.1211. [DOI] [PubMed] [Google Scholar]
  40. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase. Science. 1996 Dec 20;274(5295):2060–2063. doi: 10.1126/science.274.5295.2060. [DOI] [PubMed] [Google Scholar]
  41. Traut T. W. The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem. 1994 May 15;222(1):9–19. doi: 10.1111/j.1432-1033.1994.tb18835.x. [DOI] [PubMed] [Google Scholar]
  42. Williamson V. M., Colwell G. Acid phosphatase-1 from nematode resistant tomato : isolation and characterization of its gene. Plant Physiol. 1991 Sep;97(1):139–146. doi: 10.1104/pp.97.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Williamson V. M., Hussey R. S. Nematode pathogenesis and resistance in plants. Plant Cell. 1996 Oct;8(10):1735–1745. doi: 10.1105/tpc.8.10.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wu J., Ellison J., Salido E., Yen P., Mohandas T., Shapiro L. J. Isolation and characterization of XE169, a novel human gene that escapes X-inactivation. Hum Mol Genet. 1994 Jan;3(1):153–160. doi: 10.1093/hmg/3.1.153. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES