Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.04.2020.0071

Calcineurin-Responsive Transcription Factor CgCrzA Is Required for Cell Wall Integrity and Infection-Related Morphogenesis in Colletotrichum gloeosporioides  

Wang, Ping (Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University)
Li, Bing (College of Horticulture and Plant Protection, Yangzhou University)
Pan, Yu-Ting (Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University)
Zhang, Yun-Zhao (Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University)
Li, De-Wei (The Connecticut Agricultural Experiment Station Valley Laboratory)
Huang, Lin (Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University)
Publication Information
The Plant Pathology Journal / v.36, no.5, 2020 , pp. 385-397 More about this Journal
Abstract
The ascomycete fungus Colletotrichum gloeosporioides infects a wide range of plant hosts and causes enormous economic losses in the world. The transcription factors (TFs) play an important role in development and pathogenicity of many organisms. In this study, we found that the C2H2 TF CgCrzA is localized in both cytoplasm and nucleus under standard condition, and it translocated from cytoplasm to nucleus in a calcineurin-dependent manner. Moreover, the ΔCgCrzA was hypersensitive to cell wall perturbing agents and showed severe cell wall integrity defects. Deletion of the CgCRZA inhibited the development of invasive structures and lost pathogenicity to plant hosts. Our results suggested that calcineurin-responsive TF CgCrzA was not only involved in regulating cell wall integrity, but also in morphogenesis and virulence in C. gloeosporioides.
Keywords
anamorphic fungus; cell wall integrity; coelomycetes; transcription factor; virulence;
Citations & Related Records
연도 인용수 순위
  • Reference
1 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
2 Cyert, M. S. 2003. Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem. Biophys. Res. Commun. 311:1143-1150.   DOI
3 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. and Foster, G. D. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430.   DOI
4 Dichtl, K., Samantaray, S. and Wagener, J. 2016. Cell wall integrity signaling in human pathogenic fungi. Cell. Microbiol. 18:1228-1238.   DOI
5 Doering, T. L., Nosanchuk, J. D., Roberts, W. K. and Casadevall, A. 1999. Melanin as a potential cryptococcal defence against microbicidal proteins. Med. Mycol. 37:175-181.   DOI
6 Dubey, A. K., Barad, S., Luria, N., Kumar, D., Espeso, E. A. and Prusky, D. B. 2016. Cation-stress-responsive transcription factors SltA and CrzA regulate morphogenetic processes and pathogenicity of Colletotrichum gloeosporioides. PLoS ONE 11:e0168561.   DOI
7 Eisenman, H. C. and Casadevall, A. 2012. Synthesis and assembly of fungal melanin. Appl. Microbiol. Biotechnol. 93:931-940.   DOI
8 Englbrecht, C. C., Schoof, H. and Bohm, S. 2004. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5:39.   DOI
9 Fang, Y. L., Xia, L. M., Wang, P., Zhu, L. H., Ye, J. R. and Huang, L. 2018. The MAPKKK CgMck1 required for cell wall integrity, appressorium development, and pathogenicity in Colletotrichum gloeosporioides. Genes (Basel) 9:543.   DOI
10 Foster, A. J., Jenkinson, J. M. and Talbot, N. J. 2003. Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J. 22:225-235.   DOI
11 Garcia, R., Bermejo, C., Grau, C., Perez, R., Rodriguez-Pena, J. M., Francois, J., Nombela, C. and Arroyo, J. 2004. The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J. Biol. Chem. 279:15183-15195.   DOI
12 Garrett-Engele, P., Moilanen, B. and Cyert, M. S. 1995. Calcineurin, the $Ca^{2+}$/calmodulin-dependent protein phosphatase, is essential in yeast mutants with cell integrity defects and in mutants that lack a functional vacuolar $H^+$-ATPase. Mol. Cell. Biol. 15:4103-4114.   DOI
13 Geoghegan, I., Steinberg, G. and Gurr, S. 2017. The role of the fungal cell wall in the infection of plants. Trends Microbiol. 25:957-967.   DOI
14 Gow, N. A. R., Latge, J.-P. and Munro, C. A. 2017. The fungal cell wall structure, biosynthesis, and function. Microbiol. Spectr. 5:FUNK-0035-2016.
15 He, F., Zhang, X., Mafurah, J. J., Zhang, M., Qian, G., Wang, R., Safdar, A., Yang, X., Liu, F. and Dou, D. 2016. The transcription factor VpCRZ1 is required for fruiting body formation and pathogenicity in Valsa pyri. Microb. Pathog. 95:101-110.   DOI
16 Huang, L., Kim, K.-T., Yang, J.-Y., Song, H., Choi, G., Jeon, J., Cheong, K., Ko, J., Xu, H. and Lee, Y.-H. 2019. A highquality draft genome sequence of Colletotrichum gloeosporioides sensu stricto SMCG1#C, a causal agent of anthracnose on Cunninghamia lanceolata in China. Mol. Plant-Microbe Interact. 32:139-141.   DOI
17 Kim, S., Hu, J., Oh, Y., Park, J., Choi, J., Lee, Y.-H., Dean, R. A. and Mitchell, T. K. 2010. Combining ChIP-chip and expression profiling to model the MoCRZ1 mediated circuit for Ca/calcineurin signaling in the rice blast fungus. PLoS Pathog. 6:e1000909.   DOI
18 Lenardon, M. D., Munro, C. A. and Gow, N. A. 2010. Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol. 13:416-423.   DOI
19 Kusuya, Y., Hagiwara, D., Sakai, K., Yaguchi, T., Gonoi, T. and Takahashi, T. 2017. Transcription factor Afmac1 controls copper import machinery in Aspergillus fumigatus. Curr. Genet. 63:777-789.   DOI
20 Langner, T. and Gohre, V. 2016. Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Curr. Genet. 62:243-254.   DOI
21 Levin, D. E. 2011. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145-1175.   DOI
22 Li, B., Dong, X., Zhao, R., Kou, R., Zheng, X. and Zhang, H. 2019. The t-SNARE protein FgPep12, associated with Fg-Vam7, is essential for ascospore discharge and plant infection by trafficking $Ca^{2+}$ ATPase FgNeo1 between Golgi and endosome/vacuole in Fusarium graminearum. PLoS Pathog. 15:e1007754.   DOI
23 Madrid, M. P., Di Pietro, A. and Roncero, M. I. 2003. Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Mol. Microbiol. 47:257-266.   DOI
24 Martin-Udiroz, M., Madrid, M. P. and Roncero, M. I. 2004. Role of chitin synthase genes in Fusarium oxysporum. Microbiology (Reading) 50:3175-3187.   DOI
25 Yun, Y., Zhou, X., Yang, S., Wen, Y., You, H., Zheng, Y., Norvienyeku, J., Shim, W.-B. and Wang, Z. 2019. Fusarium oxysporum f. sp. lycopersici $C_2H_2$ transcription factor FolCzf1 is required for conidiation, fusaric acid production, and early host infection. Curr. Genet. 65:773-783.   DOI
26 Pabo, C. O. and Sauer, R. T. 1992. Transcription factors: structural families and principles of DNA recognition. Annu. Rev. Biochem. 61:1053-1095.   DOI
27 Park, H.-S., Lee, S. C., Cardenas, M. E. and Heitman, J. 2019. Calcium-calmodulin-calcineurin signaling: a globally conserved virulence cascade in eukaryotic microbial pathogens. Cell Host Microbe 26:453-462.   DOI
28 Pusztahelyi, T. 2018. Chitin and chitin-related compounds in plant-fungal interactions. Mycology 9:189-201.   DOI
29 Zhang, T., Xu, Q., Sun, X. and Li, H. 2013. The calcineurin-responsive transcription factor Crz1 is required for conidation, full virulence and DMI resistance in Penicillium digitatum. Microbiol. Res. 168:211-222.   DOI
30 Zhao, C., Jung, U. S., Garrett-Engele, P., Roe, T., Cyert, M. S. and Levin, D. E. 1998. Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin. Mol. Cell. Biol. 18:1013-1022.   DOI
31 Zhou, X., Li, G. and Xu, J.-R. 2011. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol. Biol. 722:199-212.   DOI
32 Soulie, M. C., Perino, C., Piffeteau, A., Choquer, M., Malfatti, P., Cimerman, A., Kunz, C., Boccara, M. and Vidal-Cros, A. 2006. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell. Microbiol. 8:1310-1321.   DOI
33 Ryder, L. S., Dagdas, Y. F., Mentlak, T. A., Kershaw, M. J., Thornton, C. R., Schuster, M., Chen, J., Wang, Z. and Talbot, N. J. 2013. NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc. Natl. Acad. Sci. U. S. A. 110:3179-3184.   DOI
34 Schumacher, J. 2016. DHN melanin biosynthesis in the plant pathogenic fungus Botrytis cinerea is based on two developmentally regulated key enzyme (PKS)-encoding genes. Mol. Microbiol. 99:729-748.   DOI
35 Schumacher, J., de Larrinoa, I. F. and Tudzynski, B. 2008. Calcineurin-responsive zinc finger transcription factor CRZ1 of Botrytis cinerea is required for growth, development, and full virulence on bean plants. Eukaryot. Cell 7:584-601.   DOI
36 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., Lee, S.-H., Cho, A., Lee, S., Kim, M.-G., Kim, Y., Kim, J.-E., Kim, J.-C., Choi, G. J., Yun, S.-H., Lim, J. Y., Kim, M., Lee, Y.-H., Choi, Y.-D. and Lee, Y.-W. 2011. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 7:e1002310.   DOI
37 Soriani, F. M., Malavazi, I., da Silva Ferreira, M. E., Savoldi, M., Von Zeska Kress, M. R., de Souza Goldman, M. H., Loss, O., Bignell, E. and Glodman, G. H. 2008. Functional characterization of the Aspergillus fumigatus CRZ1 homologue, CrzA. Mol. Microbiol. 67:1274-1291.   DOI
38 Soulie, M.-C., Piffeteau, A., Choquer, M., Boccara, M. and Vidal-Cros, A. 2003. Disruption of Botrytis cinerea class I chitin synthase gene Bcchs1 results in cell wall weakening and reduced virulence. Fungal Genet. Biol. 40:38-46.   DOI
39 Thompson, J. E., Fahnestock, S., Farrall, L., Liao, D. I., Valent, B. and Jordan, D. B. 2000. The second naphthol reductase of fungal melanin biosynthesis in Magnaporthe grisea. J. Biol. Chem. 275:34867-34872.   DOI
40 Stathopoulos, A. M. and Cyert, M. S. 1997. Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev. 11:3432-3444.   DOI
41 Wang, T., Ren, D., Guo, H., Chen, X., Zhu, P., Nie, H. and Xu, L. 2020. CgSCD1 is essential for melanin biosynthesis and pathogenicity of Colletotrichum gloeosporioides. Pathogens 9:141.   DOI
42 Chang, H. X., Miller, L. A. and Hartman, G. L. 2014. Melaninindependent accumulation of turgor pressure in appressoria of Phakopsora pachyrhizi. Phytopathology 104:977-984.   DOI
43 Araujo, L., Goncalves, A. E. and Stadnik, M. J. 2014. Ulvan effect on conidial germination and appressoria formation of Colletotrichum gloeosporioides. Phytoparasitica 42:631-640.   DOI
44 Bulik, D. A., Olczak, M., Lucero, H. A., Osmond, B. C., Robbins, P. W. and Specht, C. A. 2003. Chitin synthesis in Saccharomyces cerevisiae in response to supplementation of growth medium with glucosamine and cell wall stress. Eukaryot. Cell 2:886-900.   DOI
45 Cao, H., Huang, P., Zhang, L., Shi, Y., Sun, D., Yan, Y., Liu, X., Dong, B., Chen, G., Snyder, J. H., Lin, F. and Lu, J. 2016. Characterization of 47 Cys2-His2 zinc finger proteins required for the development and pathogenicity of the rice blast fungus Magnaporthe oryzae. New Phytol. 211:1035-1051.   DOI
46 Chen, L., Tong, Q., Zhang, C. and Ding, K. 2019. The transcription factor FgCrz1A is essential for fungal development, virulence, deoxynivalenol biosynthesis and stress responses in Fusarium graminearum. Curr. Genet. 65:153-166.   DOI
47 Chen, W., Provart, N. J., Glazebrook, J., Katagiri, F., Chang, H. S., Eulgem, T., Mauch, F., Luan, S., Zou, G., Whitham, S. A., Budworth, P. R., Tao, Y., Xie, Z., Chen, X., Lam, S., Kreps, J. A., Harper, J. F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, T., Dangl, J. L., Wang, X. and Zhu, T. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559-574.   DOI
48 Xu, X., Wang, Y., Tian, C. and Liang, Y. M. 2016. The Colletotrichum gloeosporioides RhoB regulates cAMP and stress response pathways and is required for pathogenesis. Fungal Genet. Biol. 96:12-24.   DOI
49 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
50 Xu, J. R., Staiger, C. J. and Hamer, J. E. 1998. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl. Acad. Sci. U. S. A. 95:12713-12718.   DOI
51 Yang, J.-Y., Fang, Y.-L., Wang, P., Ye, J.-R. and Huang, L. 2018. Pleiotropic roles of ChSat4 in asexual development, cell wall integrity maintenance, and pathogenicity in Colletotrichum higginsianum. Front. Microbiol. 9:2311.   DOI
52 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
53 Yu, X., Huo, L., Liu, H., Chen, L., Wang, Y. and Zhu, X. 2015. Melanin is required for the formation of the multi-cellular conidia in the endophytic fungus Pestalotiopsis microspora. Microbiol. Res. 179:1-11.   DOI