Abstract
Disease resistance (R) genes in plants encode products that specifically recognise incompatible pathogens and trigger a cascade of events leading to disease resistance in the host plant1. R-gene specificity is dictated by both host R genes and cognate avirulence (avr) genes in pathogens2,3. However, the basis of gene-for-gene specificity is not well understood. Here, we report the cloning of the R gene Xa27 from rice and the cognate avr gene avrXa27 from Xanthomonas oryzae pv. oryzae. Resistant and susceptible alleles of Xa27 encode identical proteins. However, expression of only the resistant allele occurs when a rice plant is challenged by bacteria harbouring avrXa27, whose product is a nuclear localized type-III effector. Induction of Xa27 occurs only in the immediate vicinity of infected tissue, whereas ectopic expression of Xa27 resulted in resistance to otherwise compatible strains of the pathogen. Thus Xa27 specificity towards incompatible pathogens involves the differential expression of the R gene in the presence of the AvrXa27 effector.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Belkhadir, Y., Subramaniam, R. & Dangl, J. L. Plant disease resistance protein signalling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7, 391–399 (2004)
Flor, H. H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296 (1971)
Martin, G. B., Bogdanove, A. J. & Sessa, G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23–61 (2003)
Greenberg, J. T. & Vinatzer, B. A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6, 20–28 (2003)
Iyer, A. S. & McCouch, S. R. The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol. Plant Microbe Interact. 17, 1348–1354 (2004)
Song, W.-Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806 (1995)
Sun, X. et al. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J. 37, 517–527 (2004)
Yoshimura, S. et al. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl Acad. Sci. USA 95, 1663–1668 (1998)
Gu, K. et al. High-resolution genetic mapping of Xa27(t), a new bacterial blight resistance gene in rice, Oryza sativa L. Theor. Appl. Genet. 108, 800–807 (2004)
Zhu, W., Yang, B., Chittoor, J. M., Johnson, L. B. & White, F. F. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol. Plant Microbe Interact. 11, 824–832 (1998)
Yang, B., Zhu, W., Johnson, L. B. & White, F. F. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent, nuclear-localized, double-stranded DNA binding protein. Proc. Natl Acad. Sci. USA 97, 9807–9812 (2000)
Schornack, S. et al. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J. 37, 46–60 (2004)
Bonas, U., Stall, R. E. & Staskawicz, B. J. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218, 127–136 (1989)
Swarup, S., De Feyter, R., Brlansky, R. H. & Gabriel, D. W. A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit canker-like lesions on citrus. Phytopathology 81, 802–809 (1991)
Levy, M., Edelbaum, O. & Sela, I. Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiol. 135, 2392–2397 (2004)
Radwan, O., Mouzeyar, S., Nicolas, P. & Bouzidi, M. F. Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopora halstedii. J. Exp. Bot. 56, 567–575 (2005)
Hopkins, C. M., White, F. F., Choi, S., Guo, A. & Leach, J. E. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 5, 451–459 (1992)
Szurek, B., Marois, E., Bonas, U. & Van den Ackerveken, G. Eukaryotic features of the Xanthomonas type III effector AvrBs3: Protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26, 523–534 (2001)
Herbers, K., Conrads-Strauch, J. & Bonas, U. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356, 172–174 (1992)
White, F. F., Yang, B. & Johnson, L. B. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3, 291–298 (2000)
Wu, A. J., Andriotis, V. M., Durrant, M. C. & Rathjen, J. P. A patch of surface-exposed residues mediates negative regulation of immune signalling by tomato Pto kinase. Plant Cell 16, 2809–2821 (2004)
Lim, M. T. & Kunkel, B. N. The Pseudomonas syringae type III effector AvrRpt2 promotes virulence independently of RIN4, a predicted virulence target in Arabidopsis thaliana. Plant J. 40, 790–798 (2004)
Belkhadir, Y., Nimchuk, Z., Hubert, D. A., Mackey, D. & Dangl, J. L. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16, 2822–2835 (2004)
Yang, B. & White, F. Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol. Plant Microbe Interact. 17, 1192–1200 (2004)
Marois, E., Van den Ackerveken, G. & Bonas, U. The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol. Plant Microbe Interact. 15, 637–646 (2002)
Stebbins, E. C. & Galán, J. A. Structural mimicry in bacterial virulence. Nature 412, 701–705 (2001)
Wang, G.-L., Holsten, T. E., Song, W.-L., Wang, H.-P. & Ronald, P. C. Construction of a rice bacterial artificial chromosome library and identification of clones linked to the Xa-21 disease resistance locus. Plant J. 7, 525–533 (1995)
Yin, Z. & Wang, G.-L. Evidence of multiple complex patterns of T-DNA integration into the rice genome. Theor. Appl. Genet. 100, 461–470 (2000)
Kauffman, H. E., Reddy, A. P. K., Hsieh, S. P. Y. & Merca, S. D. An improved technique for evaluating resistance to rice varieties of Xanthomonas oryzae pv. oryzae. Plant Dis. Rep. 57, 537–541 (1973)
Acknowledgements
We thank T. Y. Teo for technical assistance, G. S. Khush, H. Leung and R. Nelson for Xa27 germplasm, Q. Zhang and J. E. Leach for X. oryzae pv. oryzae strains, K. Shimamoto for PR1 cDNA, CAMBIA for the pC1300 vector. This work was supported by the NRI programme of the US Department of Agriculture (F.F.W.); the Kansas Agriculture Experiment Station (B.Y. and F.F.W.); the intramural research funds from Temasek Life Sciences Laboratory (Z.Y.); a competitive grant from the Agri-Food and Veterinary Authority of Singapore (Z.Y.). Author Contributions K.G., B.Y., D.T. and L.W. are all co-first authors. G.-L.W. initiated the preliminary studies of Xa27. Z.Y. designed and carried out data analysis. K.G., D.T. and L.W. conceived the experiment, and together with D.W., C.S., F.Y., Z.C. and Z.Y. carried it out. For avrXa27, B.Y., F.F.W. and Z.Y. designed and carried out data analysis, B.Y., together with D.T. and K.G., conducted the experiment. F.F.W. and Z.Y. co-wrote the paper.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
A patent on the Xa27 gene has been filed by Temasek Life Sciences Laboratory with Z.Y., G.-L.W., D.T. and K.G. as inventors.
Supplementary information
Supplementary Table S1
Xa27 transgenic lines conferring race-specific resistance to X. oryzae pv. oryzae strains. (DOC 24 kb)
Supplementary Table S2
Ectopic expression of Xa27 conferring resistance to incompatible and compatible X. oryzae pv. oryzae strains. (DOC 22 kb)
Supplementary Figure S1
Amino acid sequences of AvrXa27 and its derivatives. (DOC 871 kb)
Supplementary Figure S2
Map-based cloning of Xa27 locus. (DOC 284 kb)
Supplementary Figure S3
Alignment and conserved domains of Xa27 and its paralogs from rice cultivar Nipponbare. (DOC 545 kb)
Rights and permissions
About this article
Cite this article
Gu, K., Yang, B., Tian, D. et al. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435, 1122–1125 (2005). https://doi.org/10.1038/nature03630
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03630
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.