The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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MoJMJD6, a Nuclear Protein, Regulates Conidial Germination and Appressorium Formation at the Early Stage of Pathogenesis in Magnaporthe oryzae

  • Li Zhang (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Dong Li (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Min Lu (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Zechi Wu (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Chaotian Liu (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Yingying Shi (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Mengyu Zhang (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Zhangjie Nan (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture) ;
  • Weixiang Wang (Beijing Key Laboratory of New Technology in Agricultural Application, National Demonstration Center for Experimental Plant Production Education, Department of Agronomy, College of Plant Science and Technology, Beijing University of Agriculture)
  • Received : 2022.12.16
  • Accepted : 2023.07.01
  • Published : 2023.08.01
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Abstract

In plant-pathogen interactions, Magnaporthe oryzae causes blast disease on more than 50 species of 14 monocot plants, including important crops such as rice, millet, and most 15 recently wheat. M. oryzae is a model fungus for studying plant-microbe interaction, and the main source for fungal pathogenesis in the field. Here we report that MoJMJD6 is required for conidium germination and appressorium formation in M. oryzae. We obtained MoJMJD6 mutants (ΔMojmjd6) using a target gene replacement strategy. The MoJMD6 deletion mutants were delayed for conidium germination, glycogen, and lipid droplets utilization and consequently had decreased virulence. In the ΔMojmjd6 null mutants, global histone methyltransferase modifications (H3K4me3, H3K9me3, H3K27me3, and H3K36me2/3) of the genome were unaffected. Taken together, our results indicated that MoJMJD6 function as a nuclear protein which plays an important role in conidium germination and appressorium formation in the M. oryzae. Our work provides insights into MoJMJD6-mediated regulation in the early stage of pathogenesis in plant fungi.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (Grants 31871638 to W.W.), the Special Scientific Research Project of Beijing Agriculture University (YQ201603), the Research Fund for Academic Degree & Graduate Education of Beijing University of Agriculture (2019YJS037), the Research Fund of State Key Laboratory for Biology of Plant Diseases and Insect Pests (SKLOF202102).

References

  1. Agger, K., Cloos, P. A. C., 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
  2. Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837. https://doi.org/10.1016/j.cell.2007.05.009
  3. Cao, Z., Yin, Y., Sun, X., Han, J., Sun, Q. P., Lu, M., Pan, J. and Wang, W. 2016. An ash1-like protein MoKMT2H null mutant is delayed for conidium germination and pathogenesis in Magnaporthe oryzae. Biomed Res. Int. 2016:1575430.
  4. Chen, D., Hu, H., He, W., Zhang, S., Tang, M., Xiang, S., Liu, C., Cai, X., Hendy, A., Kamran, M., Liu, H., Zheng, L., Huang, J., Chen, X.-L. and Xing, J. 2022. Endocytic protein Pal1 regulates appressorium formation and is required for full virulence of Magnaporthe oryzae. Mol. Plant Pathol. 23:133-147. https://doi.org/10.1111/mpp.13149
  5. Chen, J., Zheng, W., Zheng, S., Zhang, D., Sang, W., Chen, X., Li, G., Lu, G. and Wang, Z. 2008. Rac1 is required for pathogenicity and Chm1-dependent conidiogenesis in rice fungal pathogen Magnaporthe grisea. PLoS Pathog. 4:e1000202.
  6. Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., An, G. and Cao, X. 2013. Control of transposon activity by a histone H3K4 demethylase in rice. Proc. Natl. Acad. Sci. U. S. A. 110:1953-1958. https://doi.org/10.1073/pnas.1217020110
  7. Gan, E.-S., Xu, Y., Wong, J.-Y., Goh, J. G., Sun, B., Wee, W.-Y., Huang, J. and Ito, T. 2014. Jumonji demethylases moderate precocious flowering at elevated temperature via regulation of FLC in Arabidopsis. Nat. Commun. 5:5098.
  8. Hamer, J. E., Valent, B. and Chumley, F. G. 1989. Mutations at the smo genetic locus affect the shape of diverse cell types in the rice blast fungus. Genetics 122:351-361. https://doi.org/10.1093/genetics/122.2.351
  9. Huang, S., Zhang, A., Jin, J. B., Zhao, B., Wang, T.-J., Wu, Y., Wang, S., Liu, Y., Wang, J., Guo, P., Ahmad, R., Liu, B. and Xu, Z.-Y. 2019. Arabidopsis histone H3K4 demethylase JMJ17 functions in dehydration stress response. New Phytol. 223:1372-1387. https://doi.org/10.1111/nph.15874
  10. Huang, Y., Chen, D., Liu, C., Shen, W. and Ruan, Y. 2016. Evolution and conservation of JmjC domain proteins in the green lineage. Mol. Genet. Genomics 291:33-49. https://doi.org/10.1007/s00438-015-1089-4
  11. 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. https://doi.org/10.5423/PPJ.OA.11.2016.0244
  12. Kankanala, P., Czymmek, K. and Valent, B. 2007. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706-724. https://doi.org/10.1105/tpc.106.046300
  13. Klose, R. J., Kallin, E. M. and Zhang, Y. 2006. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 7:715-727. https://doi.org/10.1038/nrg1945
  14. 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
  15. Lee, S. H., Farh, M. E-.A., Lee, J., Oh, Y. T., Cho, E., Park, J., Son, H. and Jeon, J. 2021. A histone deacetylase, Magnaporthe oryzae RPD3, regulates reproduction and pathogenic development in the rice blast fungus. mBio 12:e0260021.
  16. Li, G., Zhang, X., Tian, H., Choi, Y.-E., Tao, W. A. and Xu, J.-R. 2017. MST50 is involved in multiple MAP kinase signaling pathways in Magnaporthe oryzae. Environ. Microbiol. 19:1959-1974. https://doi.org/10.1111/1462-2920.13710
  17. Li, L., Xue, C., Bruno, K., Nishimura, M. and Xu, J.-R. 2004. Two PAK kinase genes, CHM1 and MST20, have distinct functions in Magnaporthe grisea. Mol. Plant-Microbe Interact. 17:547-556. https://doi.org/10.1094/MPMI.2004.17.5.547
  18. Li, Y., Zheng, X., Zhu, M., Chen, M., Zhang, S., He, F., Chen, X., Lv, J., Pei, M., Zhang, Y., Zhang, Y., Wang, W., Zhang, J., Wang, M., Wang, Z., Li, G. and Lu, G. 2019. MoIVD-mediated leucine catabolism is required for vegetative growth, conidiation and full virulence of the rice blast fungus Magnaporthe oryzae. Front. Microbiol. 10:444.
  19. Liu, P., Zhang, S., Zhou, B., Luo, X., Zhou, X. F., Cai, B., Jin, Y. H., Niu, D., Lin, J., Cao, X. and Jin, J. B. 2019. The histone H3K4 demethylase JMJ16 represses leaf senescence in Arabidopsis. Plant Cell 31:430-443. https://doi.org/10.1105/tpc.18.00693
  20. Lloret-Llinares, M., Carre, C., Vaquero, A., de Olano, N. and Azorin, F. 2008. Characterization of Drosophila melanogaster JmjC+N histone demethylases. Nucleic Acids Res. 36:2852-2863. https://doi.org/10.1093/nar/gkn098
  21. Lu, F., Cui, X., Zhang, S., 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
  22. Mosammaparast, N. and Shi, Y. 2010. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 79:155-179. https://doi.org/10.1146/annurev.biochem.78.070907.103946
  23. Odenbach, D., Breth, B., Thines, E., Weber, R. W. S., 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
  24. Park, G., Xue, C., Zhao, X., Kim, Y., Orbach, M. and Xu, J.-R. 2006. Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18:2822-2835. https://doi.org/10.1105/tpc.105.038422
  25. Peng, Y.-L. and Shishiyama, J. 1988. Temporal sequence of cytological events in rice leaves infected with Pyricularia oryzae. Can. J. Bot. 66:730-735. https://doi.org/10.1139/b88-107
  26. Pham, K. T. M., Inoue, Y., Vu, B. V., Nguyen, H. H., Nakayashiki, T., Ikeda, K.-I. and Nakayashiki, H. 2015. MoSET1 (histone H3K4 methyltransferase in Magnapothe oryzae) regulates global gene expression during infection-related morphogenesis. PLoS Genet. 11:e1005385.
  27. Pinnschmidt, H. O., Bonman, J. M. and Kranz, J. 1995. Lesion development and sporulation of rice blast. J. Plant Dis. Prot. 102:299-306.
  28. Qu, Y., Wang, J., Huang, P., Liu, X., Lu, J. and Lin, F.-C. 2021. PoRal2 is involved in appressorium formation and virulence via Pmk1 MAPK pathways in the rice blast fungus Pyricularia oryzae. Front. Plant Sci. 12:702368.
  29. Sakulkoo, W., Oses-Ruiz, M., Oliveira Garcia, E., Soanes, D. M., Littlejohn, G. R., Hacker, C., Correia, A., Valent, B. and Talbot, N. J. 2018. A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science 359:1399-1403. https://doi.org/10.1126/science.aaq0892
  30. Saze, H., Shiraishi, A., Miura, A. and Kakutani, T. 2008. Control of genic DNA methylation by a JmjC domain-containing protein in Arabidopsis thaliana. Science 319:462-465. https://doi.org/10.1126/science.1150987
  31. Searle, I. R., Pontes, O., Melnyk, C. W., Smith, L. M. and Baulcombe, D. C. 2010. JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 24:986-991. https://doi.org/10.1101/gad.579910
  32. Shi, Z. and Leung, H. 1995. Genetic analysis of sporulation in Magnaporthe grisea by chemical and insertional mutagenesis. Mol. Plant-Microbe Interact. 8:949-959. https://doi.org/10.1094/MPMI-8-0949
  33. Shimizu, M., Nakano, Y., Hirabuchi, A., Yoshino, K., Kobayashi, M., Yamamoto, K., Terauchi, R. and Saitoh, H. 2019. RNA-Seq of in planta-expressed Magnaporthe oryzae genes identifies MoSVP as a highly expressed gene required for pathogenicity at the initial stage of infection. Mol. Plant Pathol. 20:1682-1695. https://doi.org/10.1111/mpp.12869
  34. 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
  35. Valent, B. 1990. Rice blast as a model system for plant pathology. Phytopathology 80:33.
  36. Valent, B., Farrall, L. and Chumley, F. G. 1991. Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127:87-101. https://doi.org/10.1093/genetics/127.1.87
  37. Wu, J., Yamaguchi, N. and Ito, T. 2019. Histone demethylases control root elongation in response to stress-signaling hormone abscisic acid. Plant Signal. Behav. 14:1604019.
  38. Xu, J. R., Zhao, X. and Dean, R. A. 2007. From genes to genomes: a new paradigm for studying fungal pathogenesis in Magnaporthe oryzae. Adv. Genet. 57:175-218. https://doi.org/10.1016/S0065-2660(06)57005-1
  39. Yamane, K., Toumazou, C., Tsukada, Y.-I., Erdjument-Bromage, H., Tempst, P., Wong, J. and Zhang, Y. 2006. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 5:483-495. https://doi.org/10.1016/j.cell.2006.03.027
  40. Yang, J., Chen, D., Matar, K. A. O., Zheng, T., Zhao, Q., Xie, Y., Gao, X., Li, M., Wang, B. and Lu, G.-D. 2020. The deubiquitinating enzyme MoUbp8 is required for infection-related development, pathogenicity, and carbon catabolite repression in Magnaporthe oryzae. Appl. Microbiol. Biotechnol. 104:5081-5094. https://doi.org/10.1007/s00253-020-10572-5
  41. Yang, J., Zhao, X., Sun, J., Kang, Z., Ding, S., Xu, J.-R. and Peng, Y.-L. 2010. A novel protein Com1 is required for normal conidium morphology and full virulence in Magnaporthe oryzae. Mol. Plant-Microbe Interact. 23:112-123. https://doi.org/10.1094/MPMI-23-1-0112
  42. Yu, R., Shen, X., Liu, M., Liu, X., Yin, Z., Li, X., Feng, W., Hu, J., Zhang, H., Zheng, X., Wang, P. and Zhang, Z. 2021. The rice blast fungus MoRgs1 functioning in cAMP signaling and pathogenicity is regulated by casein kinase MoCk2 phosphorylation and modulated by membrane protein MoEmc2. PLoS Pathog. 17:e1009657.
  43. Zhang, L., Zhang, M., Liu C., Wu, Z., Luo, Z., Lu, M., Shi, Y., Nan, Z., Hu, D., Pan, J. and Wang, W. 2023a. A cytoplasmic protein MoJMJD3 can reduce early appressorium formation and fungal virulence in Magnaporthe oryzae. J. Phytopathol. 171:223-233. https://doi.org/10.1111/jph.13174
  44. Zhang, X., Li, D., Zhu, J., Zheng, J., Li, H., He, Q., Peng, J., Chen, S., Chen, X.-L. and Wang, W. 2023b. RNAPII degradation factor Def1 is required for development, stress response, and full virulence of Magnaporthe oryzae. J. Fungi 9:467.
  45. Zhou, S., Liu, X., Sun, W., Zhang, M., Yin, Y., Pan, S., He, D., Shen, M., Yang, J., Zheng, Q. and Wang, W. 2021. The COMPASS-like complex modulates fungal development and pathogenesis by regulating H3K4me3-mediated targeted gene expression in Magnaporthe oryzae. Mol. Plant Pathol. 22:422-439. https://doi.org/10.1111/mpp.13035