Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.02.2014.0018

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)
Publication Information
The Plant Pathology Journal / v.30, no.2, 2014 , pp. 136-150 More about this Journal
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
forkhead-box transcription factor; fungal development; Magnaporthe oryzae; pathogenicity; stress response;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 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.   DOI   ScienceOn
2 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.   DOI   ScienceOn
3 Sweigard, J. A., Chumley, F. G. and Valent, B. 1992. Disruption of a Magnaporthe grisea cutinase gene. Mol. Gen. Genet. 232:183-190.
4 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.   DOI   ScienceOn
5 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.   DOI   ScienceOn
6 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.   DOI   ScienceOn
7 Sambrook, J. and Russell, D. W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8 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.   DOI   ScienceOn
9 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.   DOI   ScienceOn
10 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.   DOI   ScienceOn
11 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.   DOI
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.   DOI
13 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.   DOI   ScienceOn
14 Ebbole, D. J. 2007. Magnaporthe as a model for understanding host-pathogen interactions. Annu. Rev. Phytopathol. 45:437- 456.   DOI   ScienceOn
15 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.   DOI   ScienceOn
16 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.   DOI   ScienceOn
17 Carlsson, P. and Mahlapuu, M. 2002. Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250:1-23.   DOI   ScienceOn
18 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.   DOI   ScienceOn
19 Talbot, N. J. 2003. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 57:177-202.   DOI   ScienceOn
20 Talbot, N. J. 1995. Having a blast: exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 3:9-16.   DOI   ScienceOn
21 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.   DOI   ScienceOn
22 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.   DOI   ScienceOn
23 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.   DOI   ScienceOn
24 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.   DOI   ScienceOn
25 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.   DOI   ScienceOn
26 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.   과학기술학회마을   DOI   ScienceOn
27 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.
28 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.   DOI
29 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.   DOI   ScienceOn
30 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.   DOI   ScienceOn
31 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.   DOI   ScienceOn
32 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.   DOI   ScienceOn
33 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.   DOI   ScienceOn
34 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.   DOI   ScienceOn
35 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.   DOI   ScienceOn
36 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.   DOI
37 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.   DOI   ScienceOn
38 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.   DOI   ScienceOn
39 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.   DOI   ScienceOn