The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Proteasome Inhibitors Affect Appressorium Formation and Pathogenicity of the Rice Blast Fungus, Magnaporthe oryzae

  • Wang, Yiming (Division of Applied Life Science (BK21 program), Gyeongsang National University) ;
  • Kim, Sang-Gon (Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Wu, Jingni (Division of Applied Life Science (BK21 program), Gyeongsang National University) ;
  • Yu, Seok (Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Kang, Kyu-Young (Division of Applied Life Science (BK21 program), Gyeongsang National University) ;
  • Kim, Sun-Tae (Department of Plant Bioscience, Pusan National University)
  • Received : 2011.05.06
  • Accepted : 2011.06.14
  • Published : 2011.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Previously, we identified the 20S proteasome ${\alpha}$-subunit of Magnaporthe oryzae (M. oryzae) induced during appressorium formation, and detected an increase in multiple protein ubiquitination during the early appressorium formation process (Kim et al., 2004). In this study, we further attempted to determine whether the proteasome is involved in the appressorium formation of M. oryzae both in vitro and in planta, using proteasome inhibitors. A significant increase in 20S proteasome during fungal germination and appressorium formation was observed using Western blot analysis with 20S proteasome antibody, demonstrating that proteasome-mediated protein degradation was involved in appressorium formation. Pharmacological analysis using proteasome inhibitors, MG-132, proteasome inhibitor I (PI) and proteasome inhibitor II (PII) revealed that germination and appressorium formation were delayed for 4 to 6 h on rice leaf wax-coated plates. Similarly, the treatment of proteasome inhibitors with fungal conidia on the rice leaf surface delayed appressorium formation and host infection processes as well. Additionally, fungal pathogenicity was strongly reduced at 4 days' postfungal infection. These data indicated that the fungal 20S proteasome might be involved in the pathogenicity of M. oryzae by the suppression of germination and appressorium formation.

Keywords

References

  1. Baumeister, W., Walz, J., Zuhl, F. and Seemuller, E. 1998. The proteasome: paradigm of self compartmentalizing protease. Cell 92:367-380. https://doi.org/10.1016/S0092-8674(00)80929-0
  2. Clague, M. J. and Urbe, S. 2010. Ubiquitin: same molecule, different degradation pathways. Cell 143:682-685. https://doi.org/10.1016/j.cell.2010.11.012
  3. Dahlmann, B., Kopp, F., Kuehn, L., Niedel, B., Pfeifer, G., Hegerl, R. and Baumeister, W. 1989. The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett. 251:125-131. https://doi.org/10.1016/0014-5793(89)81441-3
  4. Dick, S. 1979. Growth of Erysiphe germinis on artificial membranes. Physiol. Plant Pathol. 15:219-221. https://doi.org/10.1016/0048-4059(79)90071-7
  5. Dickinson, S. 1977. Studies in the physiology of obligate parasitism X. induction of responses to a thigmotropic stimulus. Phytopathol. Z. 89:97-115. https://doi.org/10.1111/j.1439-0434.1977.tb02847.x
  6. Genin, E., Reboud-Ravaux, M. and Vidal, J. 2010. Proteasome inhibitors: recent advances and new perspectives in medicinal chemistry. Curr. Top. Med. Chem. 10:232-256. https://doi.org/10.2174/156802610790725515
  7. George, N. D. and Clive, A. S. 1999. The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 27:22123-22126.
  8. Gilbert, R. D., Johnson, A. M. and Dean, R. A. 1996. Chemical signals responsible for appressorium formation in the rice blast fungus. Physiol. Mol. Plant Pathol. 48:335-346. https://doi.org/10.1006/pmpp.1996.0027
  9. Hoch, H. C. and Staples, R. C. 1987. Structural and chemical changes among the rust fungi during appressorium development. Annu. Rev. Phytopathol. 25:231-247. https://doi.org/10.1146/annurev.py.25.090187.001311
  10. Howard, R. J., Ferrari, M. A., Roach, D. H. and Money, N. P. 1991. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. U. S. A. 88:11281-11284. https://doi.org/10.1073/pnas.88.24.11281
  11. Irie, T., Matsumura, H., Terauchi, R. and Saitoh, H. 2003. Serial Analysis of Gene Expression (SAGE) of Magnaporthe grisea: genes involved in appressorium formation. Mol. Genet. Genomics 270:181-189. https://doi.org/10.1007/s00438-003-0911-6
  12. Jelitto, T. C., Page, H. A. and Read, N. D. 1994. Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus, Magnaporthe grisea. Annu. Rev. Microbiol. 50:491-512.
  13. Oku, M. and Sakai, Y. 2010. Peroxisomes as dynamic organelles: autophagic degradation. FEBS J. 277:3289-3294. https://doi.org/10.1111/j.1742-4658.2010.07741.x
  14. Park, J. Y., Jin, J., Lee, Y. W., Kang, S. and Lee, Y. H. 2009. Rice blast fungus (Magnaporthe oryzae) infects Arabidopsis via a mechanism distinct from that required for the infection of rice. Plant Physiol. 149:474-486. https://doi.org/10.1104/pp.108.129536
  15. Kawahara, H. and Yokosawa, H. 1992. Cell cycle-dependent change of proteasome distribution during embryonic development of the ascidian Halocynthia roretzi. Dev. Biol. 151:27-33. https://doi.org/10.1016/0012-1606(92)90210-8
  16. Kershaw, M. J. and Talbot, N. J. 2009. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc. Natl. Acad. Sci. U. S. A. 106:15967-15972. https://doi.org/10.1073/pnas.0901477106
  17. Kim, S. T., Yu, S., Kim, S. G., Kim, H. J., Kang, S. Y., Hwang, D. H., Jang, Y. S. and Kang, K. Y. 2004. Proteome analysis of rice blast fungus (Magnaporthe grisea) proteome during appressorium formation. Proteomics 4:3579-3587. https://doi.org/10.1002/pmic.200400969
  18. King, R. W., Deshaies, R. J., Peters, J. M. and Kirschner, M. W. 1996. How proteolysis drives the cell cycle. Science 274: 1652-1659. https://doi.org/10.1126/science.274.5293.1652
  19. Kurepa, J., Wang, S., Li, Y. and Smalle, J. 2009. Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav. 4:924-927. https://doi.org/10.4161/psb.4.10.9469
  20. Lee, Y. H. and Dean, R. A. 1993. cAMP regulates infection structure formation in the plant pathogenic fungus Magnaporthe grisea. Plant Cell 5:693-700. https://doi.org/10.1105/tpc.5.6.693
  21. Lee, Y. H. and Dean, R. A. 1994. Hydrohobicity of contact surface induces appressorium formation in Magnaporthe grisea. FEMS Microbiol. Lett. 115:71-75. https://doi.org/10.1111/j.1574-6968.1994.tb06616.x
  22. Lowe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W. and Huber, R. 1995. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268:533-539. https://doi.org/10.1126/science.7725097
  23. Marian, O., Christopher, C., Eleuteri, A. M., Kohanski, R., Kam, C. M. and Powers, J. C. 1997. Reactions of [14C]-3,4-Dichloroisocoumarin with subunits of pituitary and Spleen Multicatalytic Proteinase Complexes (proteasome). Biochemitry. 36: 13946-13953. https://doi.org/10.1021/bi970666e
  24. Nandi, D., Tahiliani, P., Kumar, A. and Chandu, D. 2006. The ubiquitin-proteasome system. J. Biosci. 31:137-55. https://doi.org/10.1007/BF02705243
  25. Nguyen, L. N., Bormann, J., Le, G. T., Stärkel, C., Olsson, S., Nosanchuk, J. D., Giese, H. and Schäfer, W. 2011. Autophagy- related lipase FgATG15 of Fusarium graminearum is important for lipid turnover and plant infection. Fungal Genet. Biol. 48:217-224. https://doi.org/10.1016/j.fgb.2010.11.004
  26. Rock, L. and Goldberg, A. L. 1999. Degradation of cell proteins and the generation of MHC class 1-presented peptides. Annu. Rev. Immunol. 17:739-779. https://doi.org/10.1146/annurev.immunol.17.1.739
  27. Shah, S. A., Potter, M. W. and Callery, M. P. 2001. Ubiquitin proteasome pathway: implications and advances in cancer therapy. Surg. Oncol. 10:43-52. https://doi.org/10.1016/S0960-7404(01)00018-4
  28. Skaar, J. R. and Pagano, M. 2009. Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr. Opin. Cell Biol. 21:816-824. https://doi.org/10.1016/j.ceb.2009.08.004
  29. Veneault-Fourrey, C., Barooah, M., Egan, M., Wakley, G. and Talbot, N. J. 2006. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312:580-583. https://doi.org/10.1126/science.1124550
  30. Xiao, J. Z., Watanabe, T., Kamakura, T., Ohshima, A. and Yamaguchi, I. 1994. Studies on cellular differentiation of Magnoporthe grisea physicochemical aspects of substratum surface in relation to appressorium formation. Physiol. Mol. Plant Pathol. 44:227-236. https://doi.org/10.1016/S0885-5765(05)80007-4
  31. Yanagawa, Y., Hasezawa, S., Kumagai, F., Oka, M., Fujimuro, M., Naito, T., Makino, T., Yokosawa, H., Tanaka, K., Komamine, A., Hashimoto, J., Sato, T. and Nakagawa, H. 2002. Cell-cycle dependent dynamic change of 26S proteasome distribution in tobacco BY-2 cells. Plant Cell Physiol. 43:604-613. https://doi.org/10.1093/pcp/pcf072
  32. Yim, K. O. and Bradford, K. J. 1998. Callose deposition is responsible for apoplastic semipermeability of the endosperm envelope of muskmelon seeds. Plant Physiol. 118:83-90. https://doi.org/10.1104/pp.118.1.83

Cited by

  1. Comparison of Different Protein Extraction Methods for Gel-Based Proteomic Analysis of Ganoderma spp. vol.35, pp.2, 2016, https://doi.org/10.1007/s10930-016-9656-z