The Plant Pathology Journal

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

DOI QR Code

Roles of Forkhead-box Transcription Factors in Controlling Development, Pathogenicity, and Stress Response in Magnaporthe oryzae

  • Park, Jaejin (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, Center for Fungal Pathogenesis, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University) ;
  • Kong, Sunghyung (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, Center for Fungal Pathogenesis, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University) ;
  • Kim, Seryun (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, Center for Fungal Pathogenesis, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University) ;
  • Kang, Seogchan (Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University) ;
  • Lee, Yong-Hwan (Department of Agricultural Biotechnology, Center for Fungal Genetic Resources, Center for Fungal Pathogenesis, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University)
  • Received : 2014.02.21
  • Accepted : 2014.04.02
  • Published : 2014.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Although multiple transcription factors (TFs) have been characterized via mutagenesis to understand their roles in controlling pathogenicity and infection-related development in Magnaporthe oryzae, the causal agent of rice blast, if and how forkhead-box (FOX) TFs contribute to these processes remain to be characterized. Four putative FOX TF genes were identified in the genome of M. oryzae, and phylogenetic analysis suggested that two of them (MoFKH1 and MoHCM1) correspond to Ascomycota-specific members of the FOX TF family while the others (MoFOX1 and MoFOX2) are Pezizomycotina-specific members. Deletion of MoFKH1 (${\Delta}Mofkh1$) resulted in reduced mycelial growth and conidial germination, abnormal septation and stress response, and reduced virulence. Similarly, ${\Delta}Mohcm1$ exhibited reduced mycelial growth and conidial germination. Conidia of ${\Delta}Mofkh1$ and ${\Delta}Mohcm1$ were more sensitive to one or both of the cell cycle inhibitors hydroxyurea and benomyl, suggesting their role in cell cycle control. On the other hand, loss of MoFOX1 (${\Delta}Mofox1$) did not show any noticeable changes in development, pathogenicity, and stress response. Deletion of MoFOX2 was not successful even after repeated attempts. Taken together, these results suggested that MoFKH1 and MoHCM1 are important in fungal development and that MoFKH1 is further implicated in pathogenicity and stress response in M. oryzae.

Keywords

References

  1. Bensen, E. S., Filler, S. G. and Berman, J. 2002. A forkhead transcription factor is important for true hyphal as well as yeast morphogenesis in Candida albicans. Eukaryot. Cell 1:787-798. https://doi.org/10.1128/EC.1.5.787-798.2002
  2. Bulmer, R., Pic-Taylor, A., Whitehall, S. K., Martin, K. A., Millar, J. B. A., Quinn, J. and Morgan, B. A. 2004. The forkhead transcription factor Fkh2 regulates the cell division cycle of Schizosaccharomyces pombe. Eukaryot. Cell 3:944-954. https://doi.org/10.1128/EC.3.4.944-954.2004
  3. Carlsson, P. and Mahlapuu, M. 2002. Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250:1-23. https://doi.org/10.1006/dbio.2002.0780
  4. Chi, M.-H., Park, S.-Y., Kim, S. and Lee, Y.-H. 2009a. A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog. 5:e1000401. https://doi.org/10.1371/journal.ppat.1000401
  5. Chi, M.-H., Park, S.-Y. and Lee, Y.-H. 2009b. 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. Choi, J., Cheong, K., Jung, K., Jeon, J., Lee, G.-W., Kang, S., Kim, S., Lee, Y.-W. and Lee, Y.-H. 2013. CFGP 2.0: a versatile web-based platform for supporting comparative and evolutionary genomics of fungi and Oomycetes. Nucleic Acids Res. 41:D714-D719. https://doi.org/10.1093/nar/gks1163
  7. Choi, J., Kim, Y., Kim, S., Park, J. and Lee, Y.-H. 2009. MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet. Biol. 46:243-254. https://doi.org/10.1016/j.fgb.2008.11.010
  8. Dean, R. A., Talbot, N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., Thon, M., Kulkarni, R., Xu, J.-R., Pan, H., Read, N. D., Lee, Y.-H., Carbone, I., Brown, D., Oh, Y. Y., Donofrio, N., Jeong, J. S., Soanes, D. M., Djonovic, S., Kolomiets, E., Rehmeyer, C., Li, W., Harding, M., Kim, S., Lebrun, M.-H., Bohnert, H., Coughlan, S., Butler, J., Calvo, S., Ma, L.-J., Nicol, R., Purcell, S., Nusbaum, C., Galagan, J. E. and Birren, B. W. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980-986. https://doi.org/10.1038/nature03449
  9. Ebbole, D. J. 2007. Magnaporthe as a model for understanding host-pathogen interactions. Annu. Rev. Phytopathol. 45:437- 456. https://doi.org/10.1146/annurev.phyto.45.062806.094346
  10. Goh, J., Kim, K. S., Park, J., Jeon, J., Park, S.-Y. and Lee, Y.-H. 2011. The cell cycle gene MoCDC15 regulates hyphal growth, asexual development and plant infection in the rice blast pathogen Magnaporthe oryzae. Fungal Genet. Biol. 48:784-792. https://doi.org/10.1016/j.fgb.2011.05.001
  11. Guo, M., Chen, Y., Du, Y., Dong, Y., Guo, W., Zhai, S., Zhang, H., Dong, S., Zhang, Z., Wang, Y., Wang, P. and Zheng, X. 2011. The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 7:e1001302. https://doi.org/10.1371/journal.ppat.1001302
  12. Hermann-Le Denmat, S., Werner, M., Sentenac, A. and Thuriaux, P. 1994. Suppression of yeast RNA polymerase III mutations by FHL1, a gene coding for a fork head protein involved in rRNA processing. Mol. Cell. Biol. 14:2905-2913. https://doi.org/10.1128/MCB.14.5.2905
  13. Horie, S., Watanabe, Y., Tanaka, K., Nishiwaki, S., Fujioka, H., Abe, H., Yamamoto, M. and Shimoda, C. 1998. The Schizosaccharomyces pombe mei4+ gene encodes a meiosis-specific transcription factor containing a forkhead DNA-binding domain. Mol. Cell. Biol. 18:2118-2129. https://doi.org/10.1128/MCB.18.4.2118
  14. Jurgens, G., Wieschaus, E., Nusslein-Volhard, C. and Kluding, H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Roux's Arch. Dev. Biol. 193:283-295. https://doi.org/10.1007/BF00848157
  15. Kim, S., Park, J., Park, S.-Y., Mitchell, T. K. and Lee, Y.-H. 2010. Identification and analysis of in planta expressed genes of Magnaporthe oryzae. BMC Genomics 11:104. https://doi.org/10.1186/1471-2164-11-104
  16. 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
  17. Koranda, M., Schleiffer, A., Endler, L. and Ammerer, G. 2000. Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters. Nature 406:94-98. https://doi.org/10.1038/35017589
  18. Kumar, R., Reynolds, D. M., Shevchenko, A., Shevchenko, A., Goldstone, S. D. and Dalton, S. 2000. Forkhead transcription factors, Fkh1p and Fkh2p, collaborate with Mcm1p to control transcription required for M-phase. Curr. Biol. 10:896-906. https://doi.org/10.1016/S0960-9822(00)00618-7
  19. Lee, B.-Y., Han, S.-Y., Choi, H. G., Kim, J. H., Han, K.-H. and Han, D.-M. 2005. Screening of growth- or development-related genes by using genomic library with inducible promoter in Aspergillus nidulans. J. Microbiol. 43:523-528.
  20. Mehrabi, R., Ding, S. and Xu, J.-R. 2008. MADS-box transcription factor Mig1 is required for infectious growth in Magnaporthe grisea. Eukaryot. Cell 7:791-799. https://doi.org/10.1128/EC.00009-08
  21. Park, J., Park, J., Jang, S., Kim, S., Kong, S., Choi, J., Ahn, K., Kim, J., Lee, S., Kim, S., Park, B., Jung, K., Kim, S., Kang, S. and Lee, Y.-H. 2008. FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors. Bioinformatics 24:1024-1025. https://doi.org/10.1093/bioinformatics/btn058
  22. Park, M.-H., Kim, H.-Y., Kim, J. H. and Han, K.-H. 2010. Gene structure and function of fkhE a forkhead gene in a filamentous fungus Aspergillus nidulans. Kor. J. Mycol. 38:160-166. https://doi.org/10.4489/KJM.2010.38.2.160
  23. Park, S.-Y., Choi, J., Lim, S.-E., Lee, G.-W., Park, J., Kim, Y., Kong, S., Kim, S., Rho, H.-S., Jeon, J., Chi, M.-H., Kim, S., Khang, C. H., Kang, S. and Lee, Y.-H. 2013. Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus. PLoS Pathog. 9:e1003350. https://doi.org/10.1371/journal.ppat.1003350
  24. Pramila, T., Wu, W., Miles, S., Noble, W. S. and Breeden, L. L. 2006. The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 20:2266-2278. https://doi.org/10.1101/gad.1450606
  25. Ribar, B., Grallert, A., Olah, E. and Szallasi, Z. 1999. Deletion of the sep1+ forkhead transcription factor homologue is not lethal but causes hyphal growth in Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun. 263:465-474. https://doi.org/10.1006/bbrc.1999.1333
  26. Sambrook, J. and Russell, D. W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  27. Saunders, D. G. O., Dagdas, Y. F. and Talbot, N. J. 2010. Spatial uncoupling of mitosis and cytokinesis during appressoriummediated plant infection by the rice blast fungus Magnaporthe oryzae. Plant Cell 22:2417-2428. https://doi.org/10.1105/tpc.110.074492
  28. Shimeld, S. M., Degnan, B. and Luke, G. N. 2010. Evolutionary genomics of the Fox genes: origin of gene families and the ancestry of gene clusters. Genomics 95:256-260. https://doi.org/10.1016/j.ygeno.2009.08.002
  29. Soanes, D. M., Chakrabarti, A., Paszkiewicz, K. H., Dawe, A. L. and Talbot, N. J. 2012. Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 8:e1002514. https://doi.org/10.1371/journal.ppat.1002514
  30. Sweigard, J. A., Chumley, F. G. and Valent, B. 1992. Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 232:183-190.
  31. Szilagyi, Z., Batta, G., Enczi, K. and Sipiczki, M. 2005. Characterisation of two novel fork-head gene homologues of Schizosaccharomyces pombe: their involvement in cell cycle and sexual differentiation. Gene 348:101-109. https://doi.org/10.1016/j.gene.2004.12.043
  32. 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
  33. Talbot, N. J. 2003. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 57:177-202. https://doi.org/10.1146/annurev.micro.57.030502.090957
  34. Talbot, N. J., Ebbole, D. J. and Hamer, J. E. 1993. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575-1590. https://doi.org/10.1105/tpc.5.11.1575
  35. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  36. Weigel, D., Jurgens, G., Kuttner, F., Seifert, E. and Jackle, H. 1989. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57:645-658. https://doi.org/10.1016/0092-8674(89)90133-5
  37. 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
  38. Yu, J.-H., Hamari, Z., Han, K.-H., Seo, J.-A., Reyes-Dominguez, Y. and Scazzocchio, C. 2004. Double-joint PCR: a PCRbased molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41:973-981. https://doi.org/10.1016/j.fgb.2004.08.001
  39. Zhu, G., Spellman, P. T., Volpe, T., Brown, P. O., Botstein, D., Davis, T. N. and Futcher, B. 2000. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406:90-94. https://doi.org/10.1038/35017581

Cited by

  1. Genome-Wide Analysis of Hypoxia-Responsive Genes in the Rice Blast Fungus, Magnaporthe oryzae vol.10, pp.8, 2015, https://doi.org/10.1371/journal.pone.0134939
  2. Genome-wide analyses of DNA-binding proteins harboring AT-hook motifs and their functional roles in the rice blast pathogen, Magnaporthe oryzae vol.36, pp.6, 2014, https://doi.org/10.1007/s13258-014-0233-6
  3. PcFKH1, a novel regulatory factor from the forkhead family, controls the biosynthesis of penicillin in Penicillium chrysogenum vol.115, 2015, https://doi.org/10.1016/j.biochi.2015.05.015
  4. Role of theMoYAK1protein kinase gene inMagnaporthe oryzaedevelopment and pathogenicity vol.17, pp.11, 2015, https://doi.org/10.1111/1462-2920.13010
  5. An atypical forkhead-containing transcription factor SsFKH1 is involved in sclerotial formation and is essential for pathogenicity in Sclerotinia sclerotiorum vol.18, pp.7, 2017, https://doi.org/10.1111/mpp.12453
  6. The Sclerotinia sclerotiorum FoxE2 Gene Is Required for Apothecial Development vol.106, pp.5, 2016, https://doi.org/10.1094/PHYTO-08-15-0181-R
  7. Large-scale molecular genetic analysis in plant-pathogenic fungi: a decade of genome-wide functional analysis vol.18, pp.5, 2017, https://doi.org/10.1111/mpp.12497
  8. Distinct roles of the YPEL gene family in development and pathogenicity in the ascomycete fungus Magnaporthe oryzae vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-32633-6