The Plant Pathology Journal

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

DOI QR Code

A Putative Transcription Factor pcs1 Positively Regulates Both Conidiation and Sexual Reproduction in the Cereal Pathogen Fusarium graminearum

  • Jung, Boknam (Department of Applied Biology, Dong-A University) ;
  • Park, Jungwook (Department of Microbiology, Pusan National University) ;
  • Son, Hokyoung (Department of Agricultural Biotechnology and Center for Fungal Pathogenesis, Seoul National University) ;
  • Lee, Yin-Won (Department of Agricultural Biotechnology and Center for Fungal Pathogenesis, Seoul National University) ;
  • Seo, Young-Su (Department of Microbiology, Pusan National University) ;
  • Lee, Jungkwan (Department of Applied Biology, Dong-A University)
  • Received : 2014.04.21
  • Accepted : 2014.06.12
  • Published : 2014.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

The plant pathogen Fusarium graminearum causes Fusarium head blight in cereal crops and produces mycotoxins that are harmful to animals and humans. For the initiation and spread of disease, asexual and sexual reproduction is required. Therefore, studies on fungal reproduction contribute to the development of new methods to control and maintain the fungal population. Screening a previously generated transcription factor mutant collection, we identified one putative $C_2H_2$ zincfinger transcription factor, pcs1, which is required for both sexual and asexual reproduction. Deleting pcs1 in F. graminearum resulted in a dramatic reduction in conidial production and a complete loss of sexual reproduction. The pathways and gene ontology of pcs1-dependent genes from microarray experiments showed that several G-protein related pathways, oxidase activity, ribosome biogenesis, and RNA binding and processing were highly enriched, suggesting that pcs1 is involved in several different biological processes. Further, overexpression of pcs1 increased conidial production and resulted in earlier maturation of ascospores compared to the wild-type strain. Additionally, the vegetative growth of the overexpression mutants was decreased in nutrient-rich conditions but was not different from the wild-type strain in nutrient-poor conditions. Overall, we discovered that the pcs1 transcription factor positively regulates both conidiation and sexual reproduction and confers nutrient condition-dependent vegetative growth.

Keywords

References

  1. Bowden, R. L. and Leslie, J. F. 1999. Sexual recombination in Gibberella zeae. Phytopathology 89:182-188. https://doi.org/10.1094/PHYTO.1999.89.2.182
  2. Capellini, R. and Peterson, J. 1965. Macroconidium formation in submerged cultures by non-sporulating strains of Gibberella zeae. Mycologia 57:962-966. https://doi.org/10.2307/3756895
  3. Fernando, W. G. D., Paulitz, T. C., Seaman, W. L., Dutilleul, P. and Miller, J. D. 1997. Head blight gradients caused by Gibberella zeae from area sources of inoculums in wheat field plots. Phytopathology 87:414-421. https://doi.org/10.1094/PHYTO.1997.87.4.414
  4. Guenther, J. C. and Trail, F. 2005. The development and differentiation of Gibberella zeae (anamorph: Fusarium graminearum) during colonization of wheat. Mycologia 97:229-237. https://doi.org/10.3852/mycologia.97.1.229
  5. Hallen, H. E., Huebner, M., Shiu, S.-H., Guldener, U. and Trail, F. 2007. Gene expression shifts during perithecium development in Gibberella zeae (anamorph Fusarium graminearum), with particular emphasis on ion transport proteins. Fungal Genet. Biol. 44:1146-1156. https://doi.org/10.1016/j.fgb.2007.04.007
  6. Han, Y.-K., Kim, M.-D., Lee, S.-H., Yun, S.-H. and Lee, Y.-W. 2007. A novel F-box protein involved in sexual development and pathogenesis in Gibberella zeae. Mol. Microbiol. 63:768-779.
  7. Harris, S. D. 2005. Morphogenesis in germinating Fusarium graminearum macroconidia. Mycologia 97:880-887. https://doi.org/10.3852/mycologia.97.4.880
  8. Hong, S.-Y., So, J., Lee, J., Min, K., Son, H., Park, C., Yun, S.- H. and Lee, Y.-W. 2010. Functional analyses of two syntaxinlike SNARE genes, GzSYN1 and GzSYN2, in the ascomycete Gibberella zeae. Fungal Genet. Biol. 47:364-372. https://doi.org/10.1016/j.fgb.2010.01.005
  9. Horwitz, B. A., Sharon, A., Lu, S.-W., Ritter, V., Sandrock, T. M., Yoder, O. C. and Turgeon, B. G. 1999. A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation. Fungal Genet. Biol. 26:19-32. https://doi.org/10.1006/fgbi.1998.1094
  10. Hou, Z., Xue, C., Peng, Y., Katan, T., Kistler, H. C. and Xu, J.- R. 2002. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant- Microbe Interact. 15:1119-1127. https://doi.org/10.1094/MPMI.2002.15.11.1119
  11. Lee, J., Chang, I.-Y., Kim, H., Yun, S.-H., Leslie, J. F. and Lee, Y.-W. 2009. Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Appl. Environ. Microbiol. 75:3289-3295. https://doi.org/10.1128/AEM.02287-08
  12. Lee, J., Kim, H., Jeon, J.-J., Kim, H.-S., Zeller, K. A., Carter, L. L. A., Leslie, J. F. and Lee, Y.-W. 2012. Population structure of and mycotoxin production by Fusarium graminearum from maize in South Korea. Appl. Environ. Microbiol. 78:2161-2167. https://doi.org/10.1128/AEM.07043-11
  13. Lee, J., Lee, T., Lee, Y.-W., Yun, S.-H. and Turgeon, B. G. 2003. Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol. Microbiol. 50:145-152. https://doi.org/10.1046/j.1365-2958.2003.03694.x
  14. Lee, J., Leslie, J. F. and Bowden, R. L. 2008. Expression and function of sex pheromones and receptors in the homothallic ascomycete Gibberella zeae. Eukaryot. Cell 7:1211-1221. https://doi.org/10.1128/EC.00272-07
  15. Lee, J., Myong, K., Kim, J.-E., Kim, H.-K., Yun, S.-H. and Lee, Y.-W. 2012. FgVelB globally regulates sexual reproduction, mycotoxin production and pathogenicity in the cereal pathogen Fusarium graminearum. Microbiology 158:1723-1733. https://doi.org/10.1099/mic.0.059188-0
  16. Lee, J., Park, C., Kim, J.-C., Kim, J. E. and Lee, Y.-W. 2010. Identification and functional characterization of genes involved in the sexual reproduction of the ascomycete fungus Gibberella zeae. Biochem. Biophys. Res. Commun. 401:48-52. https://doi.org/10.1016/j.bbrc.2010.09.005
  17. Lee, S. H., Lee, J., Lee, S., Park, E.-H., Kim, K.-W., Kim, M.- D., Yun, S.-H. and Lee, Y.-W. 2009. GzSNF1 is required for normal sexual and asexual development in the ascomycete Gibberella zeae. Eukaryot. Cell 8:116-127. https://doi.org/10.1128/EC.00176-08
  18. Lee, S., Son, H., Lee, J., Min, G., Choi, K. J., Kim, J.-C. and Lee, Y.-W. 2011. Functional analyses of two acetyl coenzyme A synthetases in the ascomycete Gibberella zeae. Eukaryot. Cell 10:1043-1052. https://doi.org/10.1128/EC.05071-11
  19. Leslie, J. F. and Summerell, B. A. 2006. The Fusarium laboratory manual. Blackwell Professional, Ames, IA, USA.
  20. Lin, Y., Son, H., Lee, J., Min, K., Choi, G. J., Kim, J.-C. and Lee, Y.-W. 2011. A putative transcription factor MYT1 is required for female fertility in the ascomycete Gibberella zeae. PLoS ONE 6:e25586. https://doi.org/10.1371/journal.pone.0025586
  21. Min, K., Lee, J., Kim, J.-C., Kim, S. G., Kim, Y. H., Vogel, S., Trail, F. and Lee, Y.-W. 2010. A novel gene, ROA, is required for normal morphogenesis and discharge of ascospores in Gibberella zeae. Eukaryot. Cell 9:1495-1503. https://doi.org/10.1128/EC.00083-10
  22. Ohara, T. and Tsuge, T. 2004. FoSTUA, encoding a basin helixloop- helix protein, differentially regulates development of three kinds of asexual spores, macroconidia, microconidia, and chlamydospores, in the fungal plant pathogen Fusarium oxysporum. Eukaryot. Cell 3:1412-1422. https://doi.org/10.1128/EC.3.6.1412-1422.2004
  23. Qi, W., Kwon, C. and Trail, F. 2006. Microarray analysis of transcript accumulation during perithecium development in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Mol. Genet. Genomics 276:87-100. https://doi.org/10.1007/s00438-006-0125-9
  24. Sambrook, J. and Russell, D. W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
  25. Seong, K.-Y., Zhao, X., Xu, J.-R., Guldener, U. and Kostler, H. C. 2008. Conidial germination in the filamentous fungus Fusarium graminearum. Fungal Genet. Biol. 45:389-399. https://doi.org/10.1016/j.fgb.2007.09.002
  26. Son, H., Lee, J., Park, A. R. and Lee, Y.-W. 2011a. ATP citrate lyase is required for normal sexual and asexual development in Gibberella zeae. Fungal Genet. Biol. 48:408-417. https://doi.org/10.1016/j.fgb.2011.01.002
  27. Son, H., Seo, Y.-S., Min, K., Park, A. R., Lee, J., Jin, J. M., Lin, Y., Cao, P., Hong, S.-Y., Kim, E. K. et al. 2011b. A phenomebased functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 7:e1002310. https://doi.org/10.1371/journal.ppat.1002310
  28. Yu, H.-Y., Seo, J.-A., Kim, J.-E., Han, K.-H., Shim, W.-B., Yun, S.-H. and Lee, Y.-W. 2008. Functional analyses of heterotrimeric G protein G$\alpha$ and G$\beta$ subunits in Gibberella zeae. Microbiology 154:392-401. https://doi.org/10.1099/mic.0.2007/012260-0
  29. 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
  30. Sutton, J. C. 1982. Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can. J. Plant Pathol. 4:195-209. https://doi.org/10.1080/07060668209501326
  31. Zeller, K. A., Bowden, R. L. and Leslie, J. F. 2003. Diversity of epidemic populations of Gibberella zeae from small quadrats in Kansas and North Dakota. Phytopathology 93:874-880. https://doi.org/10.1094/PHYTO.2003.93.7.874
  32. Zeller, K. A., Bowden, R. L. and Leslie, J. F. 2004. Population differentiation and recombination in wheat scab populations of Gibberella zeae from the United States. Mol. Ecol. 13:563-571. https://doi.org/10.1046/j.1365-294X.2004.02098.x
  33. Zenczmionka, N. J., Maier, F. J., Losch, A. P. and Schafer, W. 2003. Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr. Genet. 43:87-95.

Cited by

  1. FgSsn3 kinase, a component of the mediator complex, is important for sexual reproduction and pathogenesis in Fusarium graminearum vol.6, pp.1, 2016, https://doi.org/10.1038/srep22333