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A histone deacetylase, MoHOS2 regulates asexual development and virulence in the rice blast fungus

  • Microbial Pathogenesis and Host-Microbe Interaction
  • Published:
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Abstract

Histone acetylation/deacetylation represent a general and efficient epigenetic mechanism through which fungal cells control gene expression. Here we report developmental requirement of MoHOS2-mediated histone deacetylation (HDAC) for the rice blast fungus, Magnaporthe oryzae. Structural similarity and nuclear localization indicated that MoHOS2 is an ortholog of Saccharomyces cerevisiae Hos2, which is a member of class I histone deacetylases and subunit of Set3 complex. Deletion of MoHOS2 led to 25% reduction in HDAC activity, compared to the wild-type, confirming that it is a bona-fide HDAC. Lack of MoHOS2 caused decrease in radial growth and impinged dramatically on asexual sporulation. Such reduction in HDAC activity and phenotypic defects of ΔMohos2 were recapitulated by a single amino acid change in conserved motif that is known to be important for HDAC activity. Expression analysis revealed up-regulation of MoHOS2 and concomitant down-regulation of some of the key genes involved in asexual reproduction under sporulation-promoting condition. In addition, the deletion mutant exhibited defect in appressorium formation from both germ tube tip and hyphae. As a result, ΔMohos2 was not able to cause disease symptoms. Wound-inoculation showed that the mutant is compromised in its ability to grow inside host plants as well. We found that some of ROS detoxifying genes and known effector genes are de-regulated in the mutant. Taken together, our data suggest that MoHOS2-dependent histone deacetylation is pivotal for proper timing and induction of transcription of the genes that coordinate developmental changes and host infection in M. oryzae.

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References

  • Adachi, N., Kimura, A., and Horikoshi, M. 2002. A conserved motif common to the histone acetyltransferase Esa1 and the histone deacetylase Rpd3. J. Biol. Chem.277, 35688–35695.

    Article  CAS  Google Scholar 

  • Bannister, A.J. and Kouzarides, T. 2011. Regulation of chromatin by histone modifications. Cell Res.21, 381–395.

    Article  CAS  Google Scholar 

  • Brosch, G., Loidl, P., and Graessle, S. 2008. Histone modifications and chromatin dynamics: A focus on filamentous fungi. FEMS Microbiol. Rev.32, 409–439.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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., et al. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol.13, 414–430.

    Article  Google Scholar 

  • Ding, S.L., Liu, W., Iliuk, A., Ribot, C., Vallet, J., Tao, A., Wang, Y., Lebrun, M.H., and Xu, J.R. 2010. The Tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell22, 2495–2508.

    Article  CAS  Google Scholar 

  • Elias-Villalobos, A., Fernandez-Alvarez, A., Moreno-Sanchez, I., Helmlinger, D., and Ibeas, J.I. 2015. The Hos2 histone deacetylase controls ustilago maydis virulence through direct regulation of mating-type genes. PLoS Pathog.11, e1005134.

    Article  Google Scholar 

  • Fernandez, J. and Orth, K. 2018. Rise of a cereal killer: The biology of Magnaporthe oryzae biotrophic growth. Trends Microbiol.26, 582–597.

    Article  CAS  Google Scholar 

  • Grewal, C., Hickmott, J., Rentas, S., and Karagiannis, J. 2012. A conserved histone deacetylase with a role in the regulation of cytokinesis in Schizosaccharomyces pombe. Cell Div.7, 13.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Huh, A., Dubey, A., Kim, S., Jeon, J., and Lee, Y.H. 2017. MoJMJ1, encoding a histone demethylase containing JmjC domain, is required for pathogenic development of the rice blast fungus, Magnaporthe oryzae. Plant Pathol. J.33, 193–205.

    Article  CAS  Google Scholar 

  • Huh, A., Dubey, A., Kim, S., Jeon, J., and Lee, Y.H. 2014. Histone acetylation in fungal pathogens of plants. Plant Pathol. J.30, 1–9.

    Article  Google Scholar 

  • Huh, A., Dubey, A., Kim, S., Jeon, J., and Lee, Y.H. 2018. Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLoS Pathog.14, e1006875.

    Article  Google Scholar 

  • Kim, S., Park, S.Y., Kim, K.S., Rho, H.S., Chi, M.H., Choi, J., Park, J., Kong, S., Park, J., Goh, J., et al., Y.H. 2009. Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet.5, e1000757.

    Article  Google Scholar 

  • Kwon, S., Lee, J., Jeon, J., Kim, S., Park, S.Y., Jeon, J., and Lee, Y.H. 2018. Role of the histone acetyltransferase Rtt109 in development and pathogenicity of the rice blast fungus. Mol. Plant Microbe Interact.31, 1200–1210.

    Article  CAS  Google Scholar 

  • Lau, G.W. and Hamer, J.E. 1998. Acropetal: A genetic locus required for conidiophore architecture and pathogenicity in the rice blast fungus. Fungal Genet. Biol.24, 228–239.

    Article  CAS  Google Scholar 

  • Lee, K.K. and Workman, J.L. 2007. Histone acetyltransferase complexes: One size doesn't fit all. Nat. Rev. Mol. Cell. Biol.8, 284–295.

    Article  CAS  Google Scholar 

  • Lengeler, K.B., Davidson, R.C., D'Souza, C., Harashima, T., Shen, W.C., Wang, P., Pan, X., Waugh, M., and Heitman, J. 2000. Signal transduction cascades regulating fungal development and virulence. Microbiol. Mol. Biol. Rev.64, 746–785.

    Article  CAS  Google Scholar 

  • Li, Y., Wang, C., Liu, W., Wang, G., Kang, Z., Kistler, H.C., and Xu, J.R. 2011. The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Mol. Plant Microbe Interact.24, 487–496.

    Article  CAS  Google Scholar 

  • Matheis, S., Yemelin, A., Scheps, D., Andresen, K., Jacob, S., Thines, E., and Foster, A.J. 2017. Functions of the Magnaporthe oryzae Flb3p and Flb4p transcription factors in the regulation of conidiation. Microbiol. Res.196, 106–117.

    Article  CAS  Google Scholar 

  • Millar, C.B., Kurdistani, S.K., and Grunstein, M. 2004. Acetylation of yeast histone H4 lysine 16: A switch for protein interactions in heterochromatin and euchromatin. Cold Spring Harb. Symp. Quant. Biol.69, 193–200.

    Article  CAS  Google Scholar 

  • Mulder, N.J. and Apweiler, R. 2008. The InterPro database and tools for protein domain analysis. Curr. Protoc. Bioinformatics Chapter 2, Unit 2.7.

    Google Scholar 

  • Orbach, M.J., Farrall, L., Sweigard, J.A., Chumley, F.G., and Valent, B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell12, 2019–2032.

    Article  CAS  Google Scholar 

  • Park, J., Kim, S., Kwon, S., and Lee, Y.H. 2014. A quick and accurate screening method for fungal gene-deletion mutants by direct, priority-based, and inverse PCRs. J. Microbiol. Methods105, 39–41.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pidroni, A., Faber, B., Brosch, G., Bauer, I., and Graessle, S. 2018. A class 1 histone deacetylase as major regulator of secondary metabolite production in Aspergillus nidulans. Front. Microbiol.9, 2212.

    Article  Google Scholar 

  • Pijnappel, W.W., Schaft, D., Roguev, A., Shevchenko, A., Tekotte, H., Wilm, M., Rigaut, G., Seraphin, B., Aasland, R., and Stewart, A.F. 2001. The S. cerevisiae Set3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev.15, 2991–3004.

    Article  CAS  Google Scholar 

  • Rundlett, S.E., Carmen, A.A., Kobayashi, R., Bavykin, S., Turner, B.M., and Grunstein, M. 1996. Hda1 and Rpd3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. USA93, 14503–14508.

    Article  CAS  Google Scholar 

  • Ryder, L.S. and Talbot, N.J. 2015. Regulation of appressorium development in pathogenic fungi. Curr. Opin. Plant Biol.26, 8–13.

    Article  CAS  Google Scholar 

  • Selin, C., de Kievit, T.R., Belmonte, M.F., and Fernando, W.G. 2016. Elucidating the role of effectors in plant-fungal interactions: Progress and challenges. Front. Microbiol.7, 600.

    Article  Google Scholar 

  • Seto, E. and Yoshida, M. 2014. Erasers of histone acetylation: The histone deacetylase enzymes. Cold Spring Harb. Perspect. Biol.6, a018713.

    Article  Google Scholar 

  • Sievers, F. and Higgins, D.G. 2018. Clustal omega for making accurate alignments of many protein sequences. Protein Sci.27, 135–145.

    Article  CAS  Google Scholar 

  • Soyer, J.L., El Ghalid, M., Glaser, N., Ollivier, B., Linglin, J., Grandaubert, J., Balesdent, M.H., Connolly, L.R., Freitag, M., Rouxel, T., et al. 2014. Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet.10, e1004227.

    Article  Google Scholar 

  • Talbot, N.J. 2003. On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol.57, 177–202.

    Article  CAS  Google Scholar 

  • Tessarz, P. and Kouzarides, T. 2014. Histone core modifications regulating nucleosome structure and dynamics. Nat. Rev. Mol. Cell. Biol.15, 703–708.

    Article  CAS  Google Scholar 

  • Wang, A., Kurdistani, S.K., and Grunstein, M. 2002. Requirement of Hos2 histone deacetylase for gene activity in yeast. Science298, 1412–1414.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Wiren, M., Silverstein, R.A., Sinha, I., Walfridsson, J., Lee, H.M., Laurenson, P., Pillus, L., Robyr, D., Grunstein, M., and Ekwall, K. 2005. Genome-wide analysis of nucleosome density histone acetylation and hdac function in fission yeast. EMBO J.24, 2906–2918.

    Article  CAS  Google Scholar 

  • Zhang, S. and Xu, J.R. 2014. Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathog.10, e1003826.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2017R1D1A3B03033932).

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  1. Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University, Gyeongsan, 38541, Republic of Korea

    Jongjune Lee, Jae-Joon Lee & Junhyun Jeon

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  1. Jongjune Lee
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Correspondence to Junhyun Jeon.

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Lee, J., Lee, JJ. & Jeon, J. A histone deacetylase, MoHOS2 regulates asexual development and virulence in the rice blast fungus. J Microbiol. 57, 1115–1125 (2019). https://doi.org/10.1007/s12275-019-9363-5

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