Skip to main content
Log in

Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae

  • Research Papers
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Xanthomonas oryzae pv. oryzae, the causal agent of bacterial blight in rice, interacts with rice plants in a gene-for-gene manner. The specificity of the interaction is dictated by avirulence (avr) genes in the pathogen and resistance (R) genes in the host. To date, no avr genes that correspond to recessive R genes have been isolated. We isolated an avrBs3/pthA family gene, avrxa5, from our previously isolated clone p58, which was originally from strain JXOIII. The avrxa5 gene converted the PXO99A strain from compatible to incompatible in rice cultivars containing the recessive xa5 gene, but not in those containing the dominant Xa5 gene. Sequencing indicated that avrxa5, which is highly similar to members of the avrBs3/pthA family, encodes a protein of 1238 amino acid residues with a conserved carboxy-terminal region containing three nuclear localization signals and a transcription activation domain. It has 19.5 34-amino-acid direct repeats, but the 13th amino acid is missing in the fifth and ninth repetitive units. Domain swapping of the repetitive regions between avrxa5 and avrXa7 changed the avirulence specificity of the genes in xa5 and Xa7 rice lines, respectively. This indicates that avrxa5 is distinct from previously characterized avrBs3/pthA members. The specificity of avrxa5 toward recessive xa5 in rice could help us better understand the molecular mechanisms of plant-pathogen specific interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Mew T W. Current status of future prospects of research on bacterial blight of rice. Ann Rev Phytopathol, 1987, 25: 359–382 10.1146/annurev.py.25.090187.002043

    Article  Google Scholar 

  2. Ronald P C, Leung H. The Rice Genome: the most precious things are not jade and pearls. Science, 2002, 296: 58–59 1:CAS:528:DC%2BD38XivVSrurc%3D, 10.1126/science.1071337, 11935008

    Article  PubMed  CAS  Google Scholar 

  3. Chen G Y, Zou L F, Wang X P, et al. Pathogenicity determinants of Xanthomonas oryzae pv. oryzae. (in Chinese). Chin Agric Sci, 2004, 37: 1301–1307 1:CAS:528:DC%2BD28XhslWitbs%3D

    CAS  Google Scholar 

  4. Niño-Liu D O, Ronald P C, Bogdanove A J. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol, 2006, 7: 303–324 10.1111/j.1364-3703.2006.00344.x, 20507449

    Article  PubMed  Google Scholar 

  5. Iyer-Pascuzzi A S, McCouch S R. Recessive Resistance genes and the Oryza sativa-Xanthomonas oryzae pv. oryzae pathosystem. Mol Plant-Microbe Interact, 2007, 20: 731–739 1:CAS:528:DC%2BD2sXmvFanuro%3D, 10.1094/MPMI-20-7-0731, 17601161

    Article  PubMed  CAS  Google Scholar 

  6. Lee B M, Park Y J, Park D S, et al. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucl Acids Res, 2005, 33: 577–586 1:CAS:528:DC%2BD2MXhtV2qtrs%3D, 10.1093/nar/gki206, 15673718

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Ochiai H, Inoue Y, Takeya M, et al. Genome sequence of Xanthomonas oryzae pv.oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jap Agric Res Quart, 2005, 39: 275–287 1:CAS:528:DC%2BD2sXhvFKnsro%3D

    Article  CAS  Google Scholar 

  8. Salzberg S L, Sommer D D, Schatz M C, et al. Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics, 2008, 9: 204 10.1186/1471-2164-9-204, 18452608

    Article  PubMed  PubMed Central  Google Scholar 

  9. Leach J E, White F F. Bacterial avirulence genes. Ann Rev Phytopathol, 1996, 34: 153–179 1:CAS:528:DyaK28XlsFOhs7k%3D, 10.1146/annurev.phyto.34.1.153

    Article  CAS  Google Scholar 

  10. Gabriel D W. The Xanthomonas avr/pth gene family, p 39–55. In Stacey G, Keen N T. eds. Plant-microbe interact, vol 4. New York: APS Press, 1999

    Google Scholar 

  11. Bai J, Choi S H, Ponciano G, et al. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol Plant-Microbe Interact, 2000, 13: 1322–1329 1:CAS:528:DC%2BD3cXotlyiuro%3D, 10.1094/MPMI.2000.13.12.1322, 11106024

    Article  PubMed  CAS  Google Scholar 

  12. Lahaye T, Bonas U. Molecular secrets of bacterial type III effector proteins. Tren Plant Sci, 2001, 6: 479–485 1:CAS:528:DC%2BD3MXnvVensrs%3D, 10.1016/S1360-1385(01)02083-0

    Article  CAS  Google Scholar 

  13. Ponciano G, Ishihara H, Tsuyumu S, et al. Bacterial effectors in plant disease and defense: keys to durable resistance? Plant Dis, 2003, 87: 1272–1282 1:CAS:528:DC%2BD3sXptFCisb0%3D, 10.1094/PDIS.2003.87.11.1272

    Article  CAS  Google Scholar 

  14. Bonas U, Stall R E, Staskawicz B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genomics, 1989, 218: 127–136 1:CAS:528:DyaK3cXhtFejs74%3D, 10.1007/BF00330575

    Article  CAS  Google Scholar 

  15. Yang B, White F F. Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact, 2005, 18: 142–149 1:CAS:528:DC%2BD2MXptFCktA%3D%3D, 10.1094/MPMI-18-0142, 15720083

    Article  PubMed  CAS  Google Scholar 

  16. Gürlebeck D, Thieme F, Bonas U. Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol, 2006, 163: 233–255 10.1016/j.jplph.2005.11.011, 16386329

    Article  PubMed  Google Scholar 

  17. Herbers K, Strauch J C, Bonas U. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature, 1992, 356: 172–174 1:CAS:528:DyaK38XitVyru7c%3D, 10.1038/356172a0

    Article  CAS  Google Scholar 

  18. Yang Y N, Defeyter R, Gabriel D W. Host-specific symptoms and increased release of Xanthomonas citri and Xanthomonas campestris pv malvacearum from leaves are determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol Plant-Microbe Interact, 1994, 7: 345–355 1:CAS:528:DyaK2cXltlSisL0%3D

    Article  CAS  Google Scholar 

  19. White F F, Yang B, Johnson L B. Prospects for understanding avirulence gene function. Curr Opin Plant Biol, 2000, 3: 291–298 1:CAS:528:DC%2BD3cXlsV2mt7w%3D, 10.1016/S1369-5266(00)00082-0, 10873850

    Article  PubMed  CAS  Google Scholar 

  20. 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, 2002, 15: 637–646 1:CAS:528:DC%2BD38Xlt1Wkurw%3D, 10.1094/MPMI.2002.15.7.637, 12118879

    Article  PubMed  CAS  Google Scholar 

  21. Szurek B, Marois E, Bonas U, et al. 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, 2001, 26: 523–534 1:CAS:528:DC%2BD3MXlvVKhsL0%3D, 10.1046/j.0960-7412.2001.01046.x, 11439138

    Article  PubMed  CAS  Google Scholar 

  22. Büttner D, Bonas U. Getting across-bacterial type III effector proteins on their way to the plant cell. EMBO J, 2002, 21: 5313–5322 10.1093/emboj/cdf536, 12374732

    Article  PubMed  PubMed Central  Google Scholar 

  23. Szurek B, Rossier O, Hause G, et al. Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol, 2002, 46: 13–23 1:CAS:528:DC%2BD38XotFSiu7Y%3D, 10.1046/j.1365-2958.2002.03139.x, 12366827

    Article  PubMed  CAS  Google Scholar 

  24. Mudgett M B. New insight to the function of phytopathologenic bacterial type III effectors in plants. Ann Rev Plant Biol, 2005, 56: 509–531 1:CAS:528:DC%2BD2MXmtVaqsrk%3D, 10.1146/annurev.arplant.56.032604.144218

    Article  CAS  Google Scholar 

  25. Wu X M, Li X H, Xu C G, et al. Fine genetic mapping of xa24, a recessive gene for resistance against Xanthomonas oryzae pv. oryzae in rice. Theor Appl Genet, 2008, 118: 185–191 1:CAS:528:DC%2BD1cXhtlGhtLjP, 10.1007/s00122-008-0888-y, 18795250

    Article  PubMed  CAS  Google Scholar 

  26. Alfano J R, Collmer A. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol, 1997, 179: 5655–5662 1:CAS:528:DyaK2sXmt1GgsLw%3D, 9294418

    PubMed  CAS  PubMed Central  Google Scholar 

  27. Yang B, Sugio A, White F F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA, 2006, 103: 10503–10508 1:CAS:528:DC%2BD28XnsVSitbY%3D, 10.1073/pnas.0604088103, 16798873

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Yang B, White F 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, 2004, 17: 1192–1200 1:CAS:528:DC%2BD2cXptVOrtr0%3D, 10.1094/MPMI.2004.17.11.1192, 15553245

    Article  PubMed  CAS  Google Scholar 

  29. Yang B, Zhu W, Johnson L B, et al. 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, 2000, 97: 9807–9812 1:CAS:528:DC%2BD3cXmtVentbk%3D, 10.1073/pnas.170286897, 10931960

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Yoshimura S, Zhu W, Yang B, et al. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol Plant-Microbe Interact, 1998, 11: 824–832 10.1094/MPMI.1998.11.8.824

    Article  Google Scholar 

  31. Zhu W G, Yang B, Wills N, et al. The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell, 1999, 11: 1665–1674 1:CAS:528:DyaK1MXms1aiu7g%3D, 10.1105/tpc.11.9.1665, 10488234

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  32. Gu KY, Yang B, Tian D S, et al. R-gene expression induced by a type-III effector triggers disease resistance in rice. Nature, 2005, 435: 1122–1125 1:CAS:528:DC%2BD2MXltl2ntr8%3D, 10.1038/nature03630, 15973413

    Article  PubMed  CAS  Google Scholar 

  33. Yoshimura S, Yamanouchi U, Katayose Y, et al. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA, 1998, 95: 1663–1668 1:CAS:528:DyaK1cXht1Wqtbs%3D, 10.1073/pnas.95.4.1663, 9465073

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Cao Y L, Duan L, Li H J, et al. Functional analysis of Xa3/Xa26 family members in rice resistance to Xanthomonas oryzae pv. oryzae. Theor Appl Genet, 2007, 115: 887–895 10.1007/s00122-007-0615-0, 17657469

    Article  PubMed  Google Scholar 

  35. Song W Y, Wang G L, Chen L L, et al. A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science, 1995, 270: 1804–1806 1:CAS:528:DyaK2MXhtVSiurnI, 10.1126/science.270.5243.1804, 8525370

    Article  PubMed  CAS  Google Scholar 

  36. Iyer A S, McCouch S R. The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant-Microbe Interact, 2004, 17: 1348–1354 1:CAS:528:DC%2BD2cXhtVCjsLbK, 10.1094/MPMI.2004.17.12.1348, 15597740

    Article  PubMed  CAS  Google Scholar 

  37. Yuan M, Chu Z, Li X, et al. Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant Cell Physiol, 2009, 50: 947–955 1:CAS:528:DC%2BD1MXmtFSnsb0%3D, 10.1093/pcp/pcp046, 19318375

    Article  PubMed  CAS  Google Scholar 

  38. Wang G L, Ruan D L, Song W Y, et al. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell, 1998, 10: 765–779 1:CAS:528:DyaK1cXjs1ehsbo%3D, 10.1105/tpc.10.5.765, 9596635

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Sun X L, Cao Y L, Yang Z F, et al. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J, 2004, 37: 517–527 1:CAS:528:DC%2BD2cXisVWhsLs%3D, 10.1046/j.1365-313X.2003.01976.x, 14756760

    Article  PubMed  CAS  Google Scholar 

  40. Hampsey M. Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol Mol Biol Rev, 1998, 62: 465–503 1:CAS:528:DyaK1cXkt1Oitbw%3D, 9618449

    PubMed  CAS  PubMed Central  Google Scholar 

  41. Wu X M, Li Y R, Zou L F, et al. Gene-for-gene relationships between rice and diverse avrBs3/pthA avirulence genes in Xanthomonas oryzae pv. oryzae. Plant Pathol, 2007, 56: 26–34 1:CAS:528:DC%2BD2sXjtlenu7k%3D

    CAS  Google Scholar 

  42. Li P, Long J Y, Huang Y C, et al. The avrXa3 isolated from Xanthomonas oryzae pv. oryzae belongs to avrBs3 gene family and is a dual-acting avirulence gene (in Chinese). Prog Nat Sci, 2004, 14: 767–773

    Google Scholar 

  43. Jiang G H, Xia Z H, Zhou L Y, et al. Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAγ1. Mol Gen Genomics, 2006, 275: 354–366 1:CAS:528:DC%2BD28XjsVOlt7k%3D, 10.1007/s00438-005-0091-7

    Article  CAS  Google Scholar 

  44. Li Z K, Sanchez A, Angeles E, et al. Are the dominant and recessive plant disease resistance genes similar? A case study of rice R genes and Xanthomonas oryzae pv. oryzae races. Genetics, 2001, 159: 757–765 1:CAS:528:DC%2BD3MXot1SrsLo%3D, 11606550

    PubMed  CAS  PubMed Central  Google Scholar 

  45. Chen GY, Yu X J, Wang J S. Cloning and sequence analysis of hrp regulatory gene, hrpXoo, of Xanthomonas oryzaepv. oryzae (in Chinese). Chin Agri Sci, 2003, 36: 528–535 1:CAS:528:DC%2BD2MXntF2k

    CAS  Google Scholar 

  46. Sugio A, Yang B, Zhu T, et al. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIA γ and OsTFX1 during bacterial blight of rice. Proc Natl Acad Sci USA, 2007, 104: 10720–10725 1:CAS:528:DC%2BD2sXnt1ygtbg%3D, 10.1073/pnas.0701742104, 17563377

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  47. Shiotani H, Fujikawa T, Ishihara H, et al. A pthA homolog from Xanthomonas axonopodis pv. citri responsible for host-specific suppression of virulence. J Bacteriol, 2007, 189: 3271–3279 1:CAS:528:DC%2BD2sXkslGqtLs%3D, 10.1128/JB.01790-06, 17293422

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  48. Hopkins C M, White F F, Choi S H, et al. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact, 1992, 5: 451–459 1:CAS:528:DyaK2cXks12mtA%3D%3D, 1335800

    Article  PubMed  CAS  Google Scholar 

  49. Katzen F, Becker A, Ielmini MV, et al. New mobilizable vectors suitable for gene replacement in Gram-negative bacteria and their use in mapping of the 3′ end of the Xanthomonas campestris pv. campestris gum operon. Appl Environ Microbiol, 1999, 65: 278–282 1:CAS:528:DyaK1MXjvVyntg%3D%3D, 9872790

    PubMed  CAS  PubMed Central  Google Scholar 

  50. De Feyter R, Kado C I, Gabriel D W. Small, stable shuttle vectors for use in Xanthomonas. Gene, 1990, 88: 65–72 10.1016/0378-1119(90)90060-5

    Article  Google Scholar 

  51. Boch J, Scholze H, Schornack S, et al. Breaking the code of DNA-binding specificity of TAL-Type III effectors. Science, 2009, 326: 1509–1512 1:CAS:528:DC%2BD1MXhsFensbnL, 10.1126/science.1178811, 19933107

    Article  PubMed  CAS  Google Scholar 

  52. Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326: 1501 1:CAS:528:DC%2BD1MXhsFensbjP, 10.1126/science.1178817, 19933106

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to GongYou Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zou, H., Zhao, W., Zhang, X. et al. Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae. Sci. China Life Sci. 53, 1440–1449 (2010). https://doi.org/10.1007/s11427-010-4109-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-010-4109-y

Keywords

Navigation