DOI QR코드

DOI QR Code

MoJMJ1, Encoding a Histone Demethylase Containing JmjC Domain, Is Required for Pathogenic Development of the Rice Blast Fungus, Magnaporthe oryzae

  • Huh, Aram (Department of Agricultural Biotechnology, College of Agriculture and Life Science, Seoul National University) ;
  • Dubey, Akanksha (Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University) ;
  • Kim, Seongbeom (Department of Agricultural Biotechnology, College of Agriculture and Life Science, Seoul National University) ;
  • Jeon, Junhyun (Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University) ;
  • Lee, Yong-Hwan (Department of Agricultural Biotechnology, College of Agriculture and Life Science, Seoul National University)
  • Received : 2016.11.13
  • Accepted : 2017.01.07
  • Published : 2017.04.01

Abstract

Histone methylation plays important roles in regulating chromatin dynamics and transcription in eukaryotes. Implication of histone modifications in fungal pathogenesis is, however, beginning to emerge. Here, we report identification and functional analysis of a putative JmjC-domain-containing histone demethylase in Magnaporthe oryzae. Through bioinformatics analysis, we identified seven genes, which encode putative histone demethylases containing JmjC domain. Deletion of one gene, MoJMJ1, belonging to JARID group, resulted in defects in vegetative growth, asexual reproduction, appressorium formation as well as invasive growth in the fungus. Western blot analysis showed that global H3K4me3 level increased in the deletion mutant, compared to wild-type strain, indicating histone demethylase activity of MoJMJ1. Introduction of MoJMJ1 gene into ${\Delta}Mojmj1$ restored defects in pre-penetration developments including appressorium formation, indicating the importance of histone demethylation through MoJMJ1 during infection-specific morphogenesis. However, defects in penetration and invasive growth were not complemented. We discuss such incomplete complementation in detail here. Our work on MoJMJ1 provides insights into H3K4me3-mediated regulation of infection-specific development in the plant pathogenic fungus.

Keywords

References

  1. Adhvaryu, K. K., Morris, S. A., Strahl, B. D. and Selker, E. U. 2005. Methylation of histone H3 lysine 36 is required for normal development in Neurospora crassa. Eukaryot. Cell 4: 1455-1464. https://doi.org/10.1128/EC.4.8.1455-1464.2005
  2. Agger, K., Christensen, J., Cloos, P. A. and Helin, K. 2008. The emerging functions of histone demethylases. Curr. Opin. Genet. Dev. 18:159-168. https://doi.org/10.1016/j.gde.2007.12.003
  3. Agger, K., Cloos, P. A., Rudkjaer, L., Williams, K., Andersen, G., Christensen, J. and Helin, K. 2009. The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev. 23:1171-1176. https://doi.org/10.1101/gad.510809
  4. Bok, J. W., Chiang, Y. M., Szewczyk, E., Reyes-Dominguez, Y., Davidson, A. D., Sanchez, J. F., Lo, H. C., Watanabe, K., Strauss, J., Oakley, B. R., Wang, C. C. and Keller, N. P. 2009. Chromatin-level regulation of biosynthetic gene clusters. Nat. Chem. Biol. 5:462-464. https://doi.org/10.1038/nchembio.177
  5. Chi, M. H., Park, S. Y. and Lee, Y. H. 2009. A quick and safe method for fungal DNA extraction. Plant Pathol. J. 25:108-111. https://doi.org/10.5423/PPJ.2009.25.1.108
  6. Dean, R., Van Kan, J. A., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J. and Foster, G. D. 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
  7. Eissenberg, J. C., Lee, M. G., Schneider, J., Ilvarsonn, A., Shiekhattar, R. and Shilatifard, A. 2007. The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat. Struct. Mol. Biol. 14:344-346. https://doi.org/10.1038/nsmb1217
  8. Grimaldi, B., Coiro, P., Filetici, P., Berge, E., Dobosy, J. R., Freitag, M., Selker, E. U. and Ballario, P. 2006. The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol. Biol. Cell. 17:4576-4583. https://doi.org/10.1091/mbc.E06-03-0232
  9. Howard, R. J. and Valent, B. 1996. Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu. Rev. Microbiol. 50:491-512. https://doi.org/10.1146/annurev.micro.50.1.491
  10. Huarte, M., Lan, F., Kim, T., Vaughn, M. W., Zaratiegui, M., Martienssen, R. A., Buratowski, S. and Shi, Y. 2007. The fission yeast Jmj2 reverses histone H3 Lysine 4 trimethylation. J. Biol. Chem. 282:21662-21670. https://doi.org/10.1074/jbc.M703897200
  11. Iwase, S., Lan, F., Bayliss, P., de la Torre-Ubieta, L., Huarte, M., Qi, H. H., Whetstine, J. R., Bonni, A., Roberts, T. M. and Shi, Y. 2007. The X-linked mental retardation gene SMCX/ JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128:1077-1088. https://doi.org/10.1016/j.cell.2007.02.017
  12. Jeon, J., Kwon, S. and Lee, Y. H. 2014. Histone acetylation in fungal pathogens of plants. Plant Pathol. J. 30:1-9. https://doi.org/10.5423/PPJ.RW.01.2014.0003
  13. Khush, G. S. 2005. What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol. Biol. 59:1-6. https://doi.org/10.1007/s11103-005-2159-5
  14. Kim, S., Park, S. Y., Kim, K. S., Rho, H. S., Chi, M. H., Choi, J., Park, J., Kong, S., Park, J., Goh, J. and Lee, Y. H. 2009. Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet. 5:e1000757. https://doi.org/10.1371/journal.pgen.1000757
  15. Klose, R. J., Kallin, E. M. and Zhang, Y. 2006. JmjC-domaincontaining proteins and histone demethylation. Nat. Rev. Genet. 7:715-727.
  16. Kooistra, S. M. and Helin, K. 2012. Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol. 13:297-311. https://doi.org/10.1038/nrm3327
  17. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128:693-705. https://doi.org/10.1016/j.cell.2007.02.005
  18. Lee, M. G., Norman, J., Shilatifard, A. and Shiekhattar, R. 2007a. Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell 128:877-887. https://doi.org/10.1016/j.cell.2007.02.004
  19. Lee, N., Zhang, J., Klose, R. J., Erdjument-Bromage, H., Tempst, P., Jones, R. S. and Zhang, Y. 2007b. The trithoraxgroup protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nat. Struct. Mol. Biol. 14:341-343. https://doi.org/10.1038/nsmb1216
  20. Lee, S. C. and Lee, Y. H. 1998. Calcium/calmodulin-dependent signaling for appressorium formation in the plant pathogenic fungus Magnaporthe grisea. Mol. Cells 8:698-704.
  21. 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
  22. Li, B., Carey, M. and Workman, J. L. 2007. The role of chromatin during transcription. Cell 128:707-719. https://doi.org/10.1016/j.cell.2007.01.015
  23. Lu, F. L., Cui, X., Zhang, S. B., Jenuwein, T. and Cao, X. 2011. Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43:715-719. https://doi.org/10.1038/ng.854
  24. Nottke, A., Colaiacovo, M. P. and Shi, Y. 2009. Developmental roles of the histone lysine demethylases. Development 136: 879-889. https://doi.org/10.1242/dev.020966
  25. Odenbach, D., Breth, B., Thines, E., Weber, R. W., Anke, H. and Foster, A. J. 2007. The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol. Microbiol. 64:293-307. https://doi.org/10.1111/j.1365-2958.2007.05643.x
  26. Pham, K. T., Inoue, Y., Vu, B. V., Nguyen, H. H., Nakayashiki, T., Ikeda, K. and Nakayashiki, H. 2015. MoSET1 (Histone H3K4 methyltransferase in Magnaporthe oryzae) regulates global gene expression during infection-related morphogenesis. PLoS Genet. 11:e1005385. https://doi.org/10.1371/journal.pgen.1005385
  27. Secombe, J., Li, L., Carlos, L. and Eisenman, R. N. 2007. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 21:537-551. https://doi.org/10.1101/gad.1523007
  28. Seward, D. J., Cubberley, G., Kim, S., Schonewald, M., Zhang, L., Tripet, B. and Bentley, D. L. 2007. Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat. Struct. Mol. Biol. 14:240-242. https://doi.org/10.1038/nsmb1200
  29. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A. and Shi, Y. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941-953. https://doi.org/10.1016/j.cell.2004.12.012
  30. Shwab, E. K., Bok, J. W., Tribus, M., Galehr, J., Graessle, S. and Keller, N. P. 2007. Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot. Cell 6:1656-1664. https://doi.org/10.1128/EC.00186-07
  31. Smith, K. M., Phatale, P. A., Sullivan, C. M., Pomraning, K. R. and Freitag, M. 2011. Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol. Cell. Biol. 31:2528-2542. https://doi.org/10.1128/MCB.01285-10
  32. Strauss, J. and Reyes-Dominguez, Y. 2011. Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet. Biol. 48:62-69. https://doi.org/10.1016/j.fgb.2010.07.009
  33. Sun, Q. and Zhou, D. X. 2008. Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc. Natl. Acad. Sci. U. S. A. 105: 13679-13684. https://doi.org/10.1073/pnas.0805901105
  34. Talbot, N. J. 1995. Having a blast: exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 3:9-16. https://doi.org/10.1016/S0966-842X(00)88862-9
  35. Tamaru, H. and Selker, E. U. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277-283. https://doi.org/10.1038/35104508
  36. Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M. E., Borchers, C. H., Tempst, P. and Zhang, Y. 2006. Histone demethylation by a family of JmjC domain-containing proteins. Nature 439:811-816. https://doi.org/10.1038/nature04433
  37. Vu, B. V., Pham, K. T. and Nakayashiki, H. 2013. Substrateinduced transcriptional activation of the MoCel7C cellulase gene is associated with methylation of histone H3 at lysine 4 in the rice blast fungus Magnaporthe oryzae. Appl. Environ. Microbiol. 79:6823-6832. https://doi.org/10.1128/AEM.02082-13
  38. Wilson, R. A. and Talbot, N. J. 2009. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol. 7:185-195. https://doi.org/10.1038/nrmicro2032
  39. Xu, J. R. and Hamer, J. E. 1996. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10:2696-2706. https://doi.org/10.1101/gad.10.21.2696
  40. Yamane, K., Tateishi, K., Klose, R. J., Fang, J., Fabrizio, L. A., Erdjument-Bromage, H., Taylor-Papadimitriou, J., Tempst, P. and Zhang, Y. 2007. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol. Cell 25:801-812. https://doi.org/10.1016/j.molcel.2007.03.001