Skip to main content
NCBI home page
The Plant Cell logoLink to The Plant Cell
. 1999 May;11(5):781–792. doi: 10.1105/tpc.11.5.781

The Rx gene from potato controls separate virus resistance and cell death responses.

A Bendahmane 1, K Kanyuka 1, D C Baulcombe 1
PMCID: PMC144223  PMID: 10330465

Abstract

Rx-mediated extreme resistance against potato virus X in potato does not involve a necrotic hypersensitive response at the site of initial infection and thereby differs from the more usual type of disease resistance in plants. However, the Rx protein is structurally similar to products of disease resistance genes conferring the hypersensitive response. We show in both Nicotiana spp and potato that Rx has the potential to initiate a cell death response but that extreme resistance is separate and epistatic to necrosis. These data indicate that cell death and pathogen arrest are separate disease resistance responses in plants.

Full Text

The Full Text of this article is available as a PDF (384.0 KB).

Selected References

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

  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Alvarez M. E., Pennell R. I., Meijer P. J., Ishikawa A., Dixon R. A., Lamb C. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell. 1998 Mar 20;92(6):773–784. doi: 10.1016/s0092-8674(00)81405-1. [DOI] [PubMed] [Google Scholar]
  4. Angell S. M., Baulcombe D. C. Consistent gene silencing in transgenic plants expressing a replicating potato virus X RNA. EMBO J. 1997 Jun 16;16(12):3675–3684. doi: 10.1093/emboj/16.12.3675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Angell S. M., Davies C., Baulcombe D. C. Cell-to-cell movement of potato virus X is associated with a change in the size-exclusion limit of plasmodesmata in trichome cells of Nicotiana clevelandii. Virology. 1996 Feb 1;216(1):197–201. doi: 10.1006/viro.1996.0046. [DOI] [PubMed] [Google Scholar]
  6. Baulcombe D., Gilbert J., Goulden M., Köhm B., Cruz S. S. Molecular biology of resistance to potato virus X in potato. Biochem Soc Symp. 1994;60:207–218. [PubMed] [Google Scholar]
  7. Bendahmane A., Köhn B. A., Dedi C., Baulcombe D. C. The coat protein of potato virus X is a strain-specific elicitor of Rx1-mediated virus resistance in potato. Plant J. 1995 Dec;8(6):933–941. doi: 10.1046/j.1365-313x.1995.8060933.x. [DOI] [PubMed] [Google Scholar]
  8. Bevan M. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 1984 Nov 26;12(22):8711–8721. doi: 10.1093/nar/12.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dangl J. L., Dietrich R. A., Richberg M. H. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. doi: 10.1105/tpc.8.10.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delledonne M., Xia Y., Dixon R. A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature. 1998 Aug 6;394(6693):585–588. doi: 10.1038/29087. [DOI] [PubMed] [Google Scholar]
  11. Donson J., Kearney C. M., Hilf M. E., Dawson W. O. Systemic expression of a bacterial gene by a tobacco mosaic virus-based vector. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7204–7208. doi: 10.1073/pnas.88.16.7204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goulden M. G., Köhm B. A., Santa Cruz S., Kavanagh T. A., Baulcombe D. C. A feature of the coat protein of potato virus X affects both induced virus resistance in potato and viral fitness. Virology. 1993 Nov;197(1):293–302. doi: 10.1006/viro.1993.1590. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Hamilton C. M., Frary A., Lewis C., Tanksley S. D. Stable transfer of intact high molecular weight DNA into plant chromosomes. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9975–9979. doi: 10.1073/pnas.93.18.9975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hammond-Kosack K. E., Silverman P., Raskin I., Jones JDG. Race-Specific Elicitors of Cladosporium fulvum Induce Changes in Cell Morphology and the Synthesis of Ethylene and Salicylic Acid in Tomato Plants Carrying the Corresponding Cf Disease Resistance Gene. Plant Physiol. 1996 Apr;110(4):1381–1394. doi: 10.1104/pp.110.4.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Jabs T., Dietrich R. A., Dangl J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996 Sep 27;273(5283):1853–1856. doi: 10.1126/science.273.5283.1853. [DOI] [PubMed] [Google Scholar]
  18. Jones D. A., Thomas C. M., Hammond-Kosack K. E., Balint-Kurti P. J., Jones J. D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994 Nov 4;266(5186):789–793. doi: 10.1126/science.7973631. [DOI] [PubMed] [Google Scholar]
  19. Jones J. D., Shlumukov L., Carland F., English J., Scofield S. R., Bishop G. J., Harrison K. Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res. 1992 Nov;1(6):285–297. doi: 10.1007/BF02525170. [DOI] [PubMed] [Google Scholar]
  20. Kohm B. A., Goulden M. G., Gilbert J. E., Kavanagh T. A., Baulcombe D. C. A Potato Virus X Resistance Gene Mediates an Induced, Nonspecific Resistance in Protoplasts. Plant Cell. 1993 Aug;5(8):913–920. doi: 10.1105/tpc.5.8.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lamb Chris, Dixon Richard A. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):251–275. doi: 10.1146/annurev.arplant.48.1.251. [DOI] [PubMed] [Google Scholar]
  22. Leonardo E. D., Sedivy J. M. A new vector for cloning large eukaryotic DNA segments in Escherichia coli. Biotechnology (N Y) 1990 Sep;8(9):841–844. doi: 10.1038/nbt0990-841. [DOI] [PubMed] [Google Scholar]
  23. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  24. Milligan S. B., Bodeau J., Yaghoobi J., Kaloshian I., Zabel P., Williamson V. M. 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. 1998 Aug;10(8):1307–1319. doi: 10.1105/tpc.10.8.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Otsuki Y., Shimomura T., Takebe I. Tobacco mosaic virus multiplication and expression of the N gene in necrotic responding tobacco varieties. Virology. 1972 Oct;50(1):45–50. doi: 10.1016/0042-6822(72)90344-3. [DOI] [PubMed] [Google Scholar]
  27. Padgett H. S., Beachy R. N. Analysis of a tobacco mosaic virus strain capable of overcoming N gene-mediated resistance. Plant Cell. 1993 May;5(5):577–586. doi: 10.1105/tpc.5.5.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rossi M., Goggin F. L., Milligan S. B., Kaloshian I., Ullman D. E., Williamson V. M. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9750–9754. doi: 10.1073/pnas.95.17.9750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ryals J. A., Neuenschwander U. H., Willits M. G., Molina A., Steiner H. Y., Hunt M. D. Systemic Acquired Resistance. Plant Cell. 1996 Oct;8(10):1809–1819. doi: 10.1105/tpc.8.10.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Schmidt H. H., Walter U. NO at work. Cell. 1994 Sep 23;78(6):919–925. doi: 10.1016/0092-8674(94)90267-4. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Staskawicz B. J., Ausubel F. M., Baker B. J., Ellis J. G., Jones J. D. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. doi: 10.1126/science.7732374. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Warren R. F., Henk A., Mowery P., Holub E., Innes R. W. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell. 1998 Sep;10(9):1439–1452. doi: 10.1105/tpc.10.9.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]
  37. Yu I. C., Parker J., Bent A. F. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7819–7824. doi: 10.1073/pnas.95.13.7819. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES