Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (10): 2477-2487    DOI: 10.1016/S2095-3119(20)63219-1
Special Issue: 植物病理合辑Plant Protection—Plant Pathology 植物细菌真菌合辑Plant Bacteria/Fungus
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Functional characterization of the catalytic and bromodomain of FgGCN5 in development, DON production and virulence of Fusarium graminearum
WANG Qian-nan*, HUANG Pan-pan*, ZHOU Shan-yue
The Key Lab of Integrated Crop Pests Management of Shandong Province/College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
FgGCN5, a GCN5 homolog in Fusarium graminearum, plays a critical role in hyphal vegetative growth, asexual and sexual reproduction, deoxynivalenol (DON) biosynthesis and plant infection.  For nuclear localized GCN5, four conserved sequence motifs (I–IV) are presented in the catalytic domain and a bromodomain in the carboxy-terminus.  As a lysine acetyltransferase, conserved negatively charged residues are present to neutralize the protons from lysine substrates.  However, the role of conserved motifs/domains and residues in FgGCN5 are unclear.  Here, we generated deletion mutant strains for each the conserved motifs/domains and a glutamate residue 130 (E130) replacement mutant.  Deletion of each conserved motif in the catalytic domain and replacement of E130 site resulted in manifold defects in hyphae growth, asexual and sexual development, DON biosynthesis, and plant infection.  Phenotypic defects in the mutant strains were similar to deletion mutants.  The deletion of the bromodomain led a significant reduction in DON production and virulence, with no effects on hyphae growth, asexual or sexual reproduction.  FgGCN5 was further found to localize to the nucleus in conidia and hyphae cells.  In conclusion, FgGCN5 encodes a nuclear localized acetyltransferase.  The conserved motifs in the catalytic domain and E130 are essential for correct functions of the gene.  The conserved bromodomain is important for DON production and pathogen virulence.  This was the first report to identify the functions of conserved motifs/domains in FgGCN5, which will contribute to our understanding of the mechanism(s) by which FgGCN5 regulates F. graminearum
Keywords:  FgGCN5        catalytic domain        bromodomain        DON        virulence  
Received: 04 February 2020   Accepted:
Fund: This study was supported by the open project of the State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, China (CSBAA2016001).
Corresponding Authors:  Correspondence ZHOU Shan-yue, E-mail:,    
About author:  * These authors contributed equally to this study.

Cite this article: 

WANG Qian-nan, HUANG Pan-pan, ZHOU Shan-yue. 2020. Functional characterization of the catalytic and bromodomain of FgGCN5 in development, DON production and virulence of Fusarium graminearum. Journal of Integrative Agriculture, 19(10): 2477-2487.

Adnan M, Fang W, Sun P, Zheng Y, Abubakar Y, Zhang J, Lou Y, Zheng W, Lu G. 2019. R-SNARE FgSec22 is AflGcnE regulates morphogenesis, aflatoxin biosynthesis, and pathogenicity. Frontiers in Microbiology, 7, 1324.
Bennett J W, Klich M. 2003. Mycotoxins. Clinical Microbiology Reviews, 16, 497–516.
Brownell J E, Zhou J, Ranalli T, Kobayashi R, Edmondson D, Roth S, Allis C D. 1996. Tetrahymena histone acetyltransferase A: A homolog to yeast gcn5p linking histone acetylation to gene activation. Cell, 84, 843–851.
Candau R, Zhou J X, Allis C D, Berger S L. 1997. Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo. EMBO Journal, 16, 555–565.
Cánovas D, Marcos A T, Gacek A, Ramos M S, Gutiamosk G, Reyes-Domyesmos Y, Strauss J. 2014. The histone acetyltransferase gene (gcn5) plays a central role in the regulation of Aspergillus asexual development. Genetics, 197, 1175–1189.
Cao S, He Y, Hao C, Xu Y, Zhang H, Wang C, Liu H, Xu, J R. 2017. RNA editing of the AMD1 gene is important for ascus maturation and ascospore discharge in Fusarium graminearum. Scientific Reports, 7, 4617.
Cavinder B, Sikhakolli U, Fellows K M, Trail F. 2012. Sexual development and ascospore discharge in Fusarium graminearum. Journal of Visualized Experiments, 61, e3895.
Chang P, Fan X, Chen J. 2015. Function and subcellular localization of Gcn5, a histone acetyltransferase in Candida albicans. Fungal Genetics and Biology, 81, 132–141.
Chen C J, Yu J J, Bi C W, Zhang Y N, Xu J Q, Wang J X, Zhou M G. 2009. Mutations in a beta-tubulin confer resistance of Gibberella zeae to benzimidazole fungicides. Phytopathology, 99, 1403–1411.
Chen L, Tong Q, Zhang C, Ding K. 2019. The transcription factor FgCrz1A is essential for fungal development, virulence, deoxynivalenol biosynthesis and stress responses in Fusarium graminearum. Current Genetics, 65, 153.
Chen Y, Wang J, Yang N, Wen Z, Sun X, Chai Y, Ma Z. 2018. Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nature Communications, 9, 3429.
Dawson M A, Kouzarides T. 2012. Cancer epigenetics: From mechanism to therapy. Cell, 150, 12–27.
Ding S L, Mehrabi R, Koten C, Kang Z S, Wei Y D, Seong K Y, Kistler H C, Xu J R. 2009. Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryotic Cell, 8, 867–876.
Elias-Villalobos A, Barrales R, Ibeas J. 2019. Chromatin modification factors in plant pathogenic fungi: Insights from Ustilago maydis. Fungal Genetics and Biology, 129, 52–64.
Gale L R, Chen L F, Hernick C A, Takamura K, Kistler H C. 2002. Population analysis of Fusarium graminearum from wheat fields in eastern China. Phytopathology, 92, 1315–1322.
Gale L R, Ward T J, Balmas V, Kistler H C. 2007. Population subdivision of Fusarium graminearum sensu stricto in the upper midwestern United States. Phytopathology, 97, 1434–1439.
Gardiner D M, Kazan K, Manners J M. 2009. Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genetics and Biology, 46, 604–613.
Georgakopoulos T, Thireos G. 1992. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription. EMBO Journal, 11, 4145–4152.
Gomes C J, Harman M W, Centuori S M, Wolgemuth C W, Martinez J D. 2018. Measuring DNA content in live cells by fluorescence microscopy. Cell Division, 13, 6.
Gonzalez-Prieto J M, Rosas-Quijano R, Dominguez A, Ruiz-Herrera J. 2014. The UmGcn5 gene encoding histone acetyltransferase from Ustilago maydis is involved in dimorphism and virulence. Fungal Genetics and Biology, 71, 86–95.
Grant P A, Duggan L, Cote J, Roberts S M, Brownell J E, Candau R, Ohba R, Owen-Hughes T, Allis C D, Winston F, Berger S L, Workman J L. 1997. Yeast gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the saga (Spt/Ada) complex. Genes & Development, 11, 1640–1650.
Henriksen P, Wagner S  A, Weinert B T, Sharma S, Bacinskaja G, Rehman M, Juffer A H, Walther T C, Lisby M, Choudhary C. 2012. Proteome-wide analysis of lysine acetylation suggests its broad regulatory scope in Saccharomyces cerevisiae. Molecular & Cellular Proteomics, 11, 1510–1532.
Hong S Y, So J, Lee J, Min K, Son H, Park C, Yun S H, Lee Y W. 2010. Functional analyses of two syntaxin-like SNARE genes, GzSYN1 and GzSYN2, in the ascomycete Gibberella zeae. Fungal Genetics and Biology, 47, 364–372.
Hou Z M, Xue C Y, Peng Y L, Katan T, Kistler H C, Xu J R. 2002. A mitogenactivated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Molecular Plant–Microbe Interactions, 15, 1119–1127.
Howlett B J, Jonkers W, Dong Y, Broz K, Kistler H. 2012. The Wor1-like protein Fgp1 regulates pathogenicity, toxin synthesis and reproduction in the phytopathogenic fungus Fusarium graminearum. PLoS Pathogens, 8, e1002724.
Jiang C, Zhang C K, Wu C L, Sun P P, Hou R, Liu H Q, Wang C F, Xu J R. 2016. TRI6 and TRI10 play different roles in the regulation of deoxynivalenol (DON) production by cAMP signalling in Fusarium graminearum. Environmental Microbiology, 18, 3689–3701.
Kong X, van Diepeningen A D, van der Lee T A J, Waalwijk C, Xu J, Xu J, Zhang H, Chen W, Feng J. 2018. The Fusarium graminearum histone acetyltransferases are important for morphogenesis, DON biosynthesis, and pathogenicity. Frontiers in Microbiology, 9, 654. 
Kuo M H, Allis C D. 1998. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays, 20, 615–626.
Lan H, Sun R, Fan K, Yang K, Zhang F, Nie X Y, Wang X, Zhuang Z, Wang S. 2016. The Aspergillus flavus histone acetyltransferase AflGcnE regulates morphogenesis, aflatoxin biosynthesis, and pathogenicity. Frontiers in Microbiology, 7, 1324.
Lee K K, Sardiu M E, Swanson S K, Gilmore J M, Torok M, Grant P A, Florens L, Workman J L, Washburn M P. 2011. Combinatorial depletion analysis to assemble the network architecture of the SAGA and ADA chromatin remodeling complexes. Molecular Systems Biology, 7, 503.
Lee Y, Min K, Son H, Park A R, Kim J C, Choi G J, Lee Y W. 2014. ELP3 is involved in sexual and asexual  development, virulence, and the oxidative stress response in Fusarium graminearum. Molecular Plant–Microbe Interactions, 27, 1344–1355.
Li C, Zhang Y, Wang H, Chen L, Zhang J, Sun M, Xu J R, Wang C. 2018. The PKR regulatory subunit of protein kinase A (PKA) is involved in the regulation of growth, sexual and asexual development, and pathogenesis in Fusarium graminearum. Molecular Plant Pathology, 19, 909–921.
Li C H, Melesse M, Zhang S J, Hao C F, Wang C F, Zhang H C, Hall M C, Xu J R. 2015. FgCDC14 regulates cytokinesis, morphogenesis, and pathogenesis in Fusarium graminearum. Molecular Microbiology, 98, 770–786.
Li S, Lin Y C, Wang P, Zhang B, Li M, Chen S, Shi R, Tunlaya-Anukit S, Liu X, Wang Z, Dai X, Yu J, Zhou C, Liu B, Wang J P, Chiang V L, Li W. 2019. Histone acetylation cooperating with AREB1 transcription factor regulates drought response and tolerance in Populus trichocarpa. The Plant Cell, 31, 663–686.
Li Y M, Wang C F, Liu W D, Wang G H, Kang Z S, Kistler H C, Xu J R. 2011. The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Molecular Plant–Microbe Interactions, 24, 487–496.
Lin Y, Fletcher C M, Zhou J, Allis C D, Wagner G. 1999. Solution structure of the catalytic domain of GCN5 histone acetyltransferase bound to co-enzyme A. Nature, 400, 86–89.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Luo Y, Zhang H, Qi L, Zhang S, Zhou X, Zhang Y, Xu J R. 2014. FgKin1 kinase localizes to the septal pore and plays a role in hyphal growth, ascospore germination, pathogenesis, and localization of Tub1 beta-tubulins in Fusarium graminearum. New Phytologist, 204, 943–954.
Lysoe E, Seong K Y, Kistler H C. 2011. The transcriptome of Fusarium graminearum during the infection of wheat. Molecular Plant–Microbe Interactions, 24, 995–1000.
McMullen M, Bergstrom G, Wolf E D, Dill-Macky R, Hershman D, Shaner G, Sanford D V. 2012. A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Disease, 96, 1712–1728.
Pray-Grant M G, Schieltz D, McMahon S J, Wood J M, Kennedy E L, Cook R G, Workman J L, Yates J R, Grant P A. 2002. The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway.Molecular and Cellular Biology, 22, 8774–8786.
Proctor R H, Hohn T M, McCormick S P. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Molecular and Cellular Biology, 8, 593–601.
Qin J, Wu M, Zhou S. 2020. FgEaf6 regulates virulence, asexual/sexual development and conidial septation in Fusarium graminearum. Current Genetics, 66, 517–529.
Rosler S M, Kramer K, Finkemeier I, Humpf H U, Tudzynski B. 2016. The SAGA complex in the rice pathogen Fusarium fujikuroi: Structure and functional characterization. Molecular Microbiology, 102, 951–974.
Seong K, Hou Z M, Tracy M, Kistler H C, Xu J R. 2005. Random insertional mutagenesis identifies genes associated with virulence in the wheat scab fungus Fusarium graminearum. Phytopathology, 95, 744–750.
Tanner K G, Trievel R C, Kuo M H, Howard R M, Berger S L, Allis C D, Marmorstein R, Denu J M. 1999. Catalytic mechanism and function of invariant glutamic acid 173 from the histone acetyltransferase gcn5 transcriptional coactivator. Journal of Biological Chemistry, 274, 18157–18160.
Wang C F, Zhang S J, Hou R, Zhao Z T, Zheng Q, Xu Q J, Zheng D W, Wang G H, Liu H Q, Gao X L, Ma J W, Kistler H C, Kang Z S, Xu J R. 2011. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathogens, 7, e1002460.
Wang Y, Liu W, Hou Z, Wang C, Zhou X, Jonkers W, Ding S, Kistler H, Xu J R. 2011. A novel transcriptional factor important for pathogenesis and ascosporogenesis in Fusarium graminearum. Molecular Plant–Microbe Interactions, 24, 118–128.
Zhang L, Liu C, Wang L, Sun S, Liu A, Liang Y, Yu J, Dong H. 2019a. FgPEX1 and FgPEX10 are required for the maintenance of Woronin bodies and full virulence of Fusarium graminearum. Current Genetics, 65, 1383–1396.
Zhang L, Wang L, Liang Y, Yu J. 2019b. FgPEX4 is involved in development, pathogenicity, and CWI in Fusarium graminearum. Current Genetics, 65, 747.
Zheng Q, Hou R, Zhang J, Ma J, Wu Z, Wang G, Wang C, Xu J R. 2013. The MAT locus genes play different roles in sexual reproduction and pathogenesis in Fusarium graminearum. PLoS ONE, 8, e66980.
Zhou S, Wu C. 2019. Comparative acetylome analysis reveals the potential roles of lysine acetylation for DON biosynthesis in Fusarium graminearum. BMC Genomics, 20, 841.
Zhou S, Yang Q, Yin C, Liu L, Liang W. 2016. Systematic analysis of the lysine acetylome in Fusarium graminearum. BMC Genomics, 17, 1019.
Zhou X Y, Heyer C, Choi Y E, Mehrabi R, Xu J R. 2010. The CID1 cyclin C-like gene is important for plant infection in Fusarium graminearum. Fungal Genetics and Biology, 47, 143–151.
[1] SHI Dong-ya, REN Wei-chao, WANG Jin, ZHANG Jie, Jane Ifunanya MBADIANYA, MAO Xue-wei, CHEN Chang-jun. The transcription factor FgNsf1 regulates fungal development, virulence and stress responses in Fusarium graminearum[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2156-2169.
[2] TIAN Li, HUANG Cai-min, ZHANG Dan-dan, LI Ran, CHEN Jie-yin, SUN Wei-xia, QIU Nian-wei, DAI Xiao-feng. Extracellular superoxide dismutase VdSOD5 is required for virulence in Verticillium dahliae[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1858-1870.
[3] Bongekile NGOBESE, Oliver Tendayi ZISHIRI, Mohamed Ezzat EL ZOWALATY. Molecular detection of virulence genes in Campylobacter species isolated from livestock production systems in South Africa[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1656-1670.
[4] CHEN Bin, TIAN Yan-li, ZHAO Yu-qiang, WANG Yuan-jie, CHUAN Jia-cheng, LI Xiang, HU Bai-shi. Genomic characteristics of Dickeya fangzhongdai isolates from pear and the function of type IV pili in the chromosome[J]. >Journal of Integrative Agriculture, 2020, 19(4): 906-920.
[5] QIN Jia-xing, LI Bao-hua, ZHOU Shan-yue. A novel glycoside hydrolase 74 xyloglucanase CvGH74A is a virulence factor in Coniella vitis[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2725-2735.
[6] YUAN Long-yu, HAO Yuan-hao, CHEN Qiao-kui, PANG Rui, ZHANG Wen-qing. Pancreatic triglyceride lipase is involved in the virulence of the brown planthopper to rice plants[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2758-2766.
[7] ZHANG Hang, YANG Feng, LI Xin-pu, LUO Jin-yin, WANG Ling, ZHOU Yu-long, YAN Yong, WANG Xu-rong, LI Hong-sheng. Detection of antimicrobial resistance and virulence-related genes in Streptococcus uberis and Streptococcus parauberis isolated from clinical bovine mastitis cases in northwestern China[J]. >Journal of Integrative Agriculture, 2020, 19(11): 2784-2791.
[8] ZHENG Na, ZHANG Liu-ping, GE Feng-yong, HUANG Wen-kun, KONG Ling-an, PENG De-liang, LIU Shi-ming. Conidia of one Fusarium solani isolate from a soybean-production field enable to be virulent to soybean and make soybean seedlings wilted[J]. >Journal of Integrative Agriculture, 2018, 17(09): 2042-2053.
[9] LIU Tai-guo, GE Run-jing, MA Yu-tong, LIU Bo, GAO Li, CHEN Wan-quan. Population genetic structure of Chinese Puccinia triticina races based on multi-locus sequences[J]. >Journal of Integrative Agriculture, 2018, 17(08): 1779-1789.
[10] FAN Hong-jie. Advances in pathogenesis of Streptococcus suis serotype 2[J]. >Journal of Integrative Agriculture, 2017, 16(12): 2834-2847.
[11] YANG Li-ming, WANG Yi-hao, PENG Yu, MIN Jiang-tao, HANG Su-qin, ZHU Wei-yun. Genomic characterization and antimicrobial susceptibility of bovine intrauterine Escherichia coli and its relationship with postpartum uterine infections[J]. >Journal of Integrative Agriculture, 2016, 15(06): 1345-1354.
[12] WANG Ji-peng, XU You-ping, ZANG Xian-peng, LI Shuang-sheng, CAI Xin-zhong. Sclerotinia sclerotiorum virulence is affected by mycelial age via reduction in oxalate biosynthesis[J]. >Journal of Integrative Agriculture, 2016, 15(05): 1034-1045.
No Suggested Reading articles found!