The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein

Molecular Plant-Microbe Interactions

Volumn 23, Issue 1, 2010, Pages 49-57

  Catanzariti, Ann Maree ^a   Dodds, Peter N ^b   Ve, Thomas ^c   Kobe, Bostjan ^c   Ellis, Jeffrey G ^b   Staskawicz, Brian J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CSIRO   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BASIDIOMYCETES; CELL DEATH; CHEMISTRY; FLAX; GENETIC POLYMORPHISM; GENETICS; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT DISEASE; PROTEIN BINDING; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; AMINO ACIDS; BASIDIOMYCOTA; CELL DEATH; FLAX; IMMUNITY, INNATE; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT PROTEINS; POLYMORPHISM, GENETIC; PROTEIN BINDING; TWO-HYBRID SYSTEM TECHNIQUES;

LINUM USITATISSIMUM; MELAMPSORA LINI;

EID: 73949112504     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-1-0049     Document Type: Article

References (32)

1. Allen, R. L., Meitz, J. C., Baumber, R. E., Hall, S. A., Lee, S. C., Rose, L. E., and Beynon, J. L. 2008. Natural variation, reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol. Plant Pathol. 9:511-523.
2. Axtell, M. J., Chisholm, S. T., Dahlbeck, D., and Staskawicz, B. J. 2003. Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol. Microbiol. 49:1537-1546.
3. Bent, A. F., and Mackey, D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399-436.
4. Bos, J. I., Kanneganti, T. D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M. R., Birch, P. R., and Kamoun, S. 2006. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death, in Nicotiana benthamiana. Plant J. 48:165-176. (Pubitemid 44484859)
5. Caplan, J. L., Mamillapalli, P., Burch-Smith, T. M., Czymmek, K., and Dinesh-Kumar, S. P. 2008. Chloroplastic protein NRIPl mediates innate immune receptor recognition of a viral effector. Cell 132:449-462. (Pubitemid 351191994)
6. Catanzariti, A, Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., and Ellis, J. G. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243-256. (Pubitemid 43951327)
7. Catanzariti, A., Dodds, P. N., and Ellis, J. G. 2007. Avirulence proteins from haustoria-forming pathogens. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 269:181-188.
8. Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., and Zhou, J. M. 2008. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146:368-376. (Pubitemid 351230764)
9. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Hostmicrobe interactions: shaping the evolution of the plant immune response. Cell 124:803-814. (Pubitemid 43261453)
10. Deslandes, L., Olivier, J., Peeters, N., Feng, D. X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S., and Marco, Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100:8024-8029.
11. Dodds, P. N., Lawrence, G. J., Catanzariti, A., Ayliffe, M. A., and Ellis, J. G. 2004. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16:755-768.
12. Dodds, P. N., Lawrence, G. J., Catanzariti, A., Teh, T., Wang, C. I., Ayliffe, M. A., Kobe, B., and Ellis, J. G. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103:8888-8893.
13. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C. S. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45:616-629. (Pubitemid 43373712)
14. Folta-Stogniew, E., and Williams, K. 1999. Determination of molecular masses of protein in solution: implementation of an HPLC size exclusion chromatography and laser light scattering in a core laboratory. J. Biomol. Technol. 10:51-63.
15. Grouffaud, S., van West, P., Avrova, A. O., Birch, P. R., and Whisson, S. C. 2008. Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestons. Microbiology 154:3743-3751.
16. Jia, Y., McAdams, S. A., Bryan, G. T., Hershey, H. P., and Valent, B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO (Eur. Mol. Biol. Organ.) J. 19:4004-4014. (Pubitemid 30608539)
17. Kamoun, S. 2007. Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10:358-365.
18. Linding, R., Jensen, L. J., Diella, F., Bork, P., Gibson, T. J., and Russell, R. B. 2003a. Protein disorder prediction: implications for structural proteomics. Structure 11:1453-1459. (Pubitemid 37412427)
19. Linding, R., Russell, R. B., Neduva, V., and Gibson, T. J. 2003b. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31:3701-3708. (Pubitemid 37442227)
20. Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl, J. L. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell .112:379-389.
21. Martin, G. B., Bogdanove, A. J., and Sessa, G. 2003. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54:23-61.
22. Rep, M., van der Does, H. C., Meijer, M., van Wijk, R., Houterman, P. M., Dekker, H. L., de Koster, C. G., and Comelissen, B. J. 2004. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol. Microbiol. 53:1373-1383.
23. Schmidt, S. A., Williams, S. J., Wang, C. I., Sornaraj, P., James, B., Kobe, B., Dodds, P. N., Ellis, J. G., and Anderson, P. A. 2007. Purification of the M flax-rust resistance protein expressed in Pichia pastoris. Plant J. 50:1107-1117.
24. Shao, F., Golstein, C., Ade, J., Stoutemyer, M., Dixon, J. E., and Innes, R. W. 2003. Cleavage of Arabidopsis PBSl by a bacterial type III effector. Science 301:1230-1233.
25. Sreerama, N., and Woody, R. W. 2000. Estimation of protein secondary structure from circular dichroism spectra: comparison, of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287:252-260.
26. Tous, G. I., Fausnaugh, J. L., Akinyosoye, O., Lackland, H., Winter-Cash, P., Vitorica, F. J., and Stein, S. 1989. Amino acid analysis on polyvinylidene difluoride membranes. Anal. Biochem. 179:50-55.
27. Tyler, B. M. 2009. Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell Microbiol. .11:13-20.
28. Ueda, H., Yamaguchi, Y., and Sano, H. 2006. Direct interaction between, the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol. Biol. 61:31-45.
29. Van den Ackerveken, G. F., Vossen, P., and De Wit, P. J. 1993. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103:91-96.
30. Wang, C. I., Guncar, G., Forwood, J. K., Teh, T., Catanzariti, A., Lawrence, G. J., Loughlin, F. E., Mackay, J. P., Schirra, H. J., Anderson, P. A., Ellis, J. G., Dodds, P. N., and Kobe, B. 2007. Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19:2898-2912.
31. Wen, J., Arakawa, T., and Philo, J. S. 1996. Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal. Biochem. 240:155-166.
32. Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., Armstrong, M. R., Grouffaud, S., van West, P., Chapman, S., Hein, I., Toth, I. K., Pritchard, L., and Birch, P. R. 2007. A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115-118.