Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (7): 1813-1824    DOI: 10.1016/S2095-3119(19)62819-4
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 |
FgHAT2 is involved in regulating vegetative growth, conidiation, DNA damage repair, DON production and virulence in Fusarium graminearum
LÜ Wu-yun, YANG Nan, XU Zhe, DAI Han, TANG Shuai, WANG Zheng-yi
State Key Laboratory of Rice Biology & Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou 310029, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  
Histone lysine acetylation is catalyzed by acetyltransferases (HATs), which is important in regulating gene expression and physiological function in eukaryotic cells.  HATs can be classified into two main types: A- and B-type HATs.  Recently, in Fusarium graminearum, it has been reported that A-type HATs are involved in hyphal development, conidiation, sexual reproduction and virulence.  However, the biological roles of B-type HATs are unknown.  Here we report the identification and characterization of two B-type HATs (FgHat1 and FgHat2) in F. graminearum.  Targeted deletion of FgHAT1 did not result in any detectable phenotypes.  However, ΔFghat2 mutants were severely defective in vegetative growth, conidia production and morphogenesis, deoxynivalenol (DON) biosynthesis and virulence.  Interestingly, deletion of FgHAT2 resulted in significantly increased sensitivity to the DNA-damaging agent methyl methanesulfonate (MMS).  Furthermore, double deletion mutants (ΔFghat1ΔFghat2) displayed similar phenotypes to the ΔFghat2 mutants.  Taken together, we conclude that FgHat2 but not FgHat1 plays essential roles in regulating morphogenesis, DNA damage repair, DON production and virulence in F. graminearum.
 
Keywords:  Fusarium graminearum        acetyltransferases        FgHAT2        pathogenicity  
Received: 14 June 2019   Accepted:
Fund: This work was supported by the National Key Basic Research and Development Program of China (2013CB127802).
Corresponding Authors:  Correspondence WANG Zheng-yi, Mobile: +86-18067908283, E-mail: zhywang@zju.edu.cn    
About author:  Lü Wu-yun, Mobile: +86-15336512118, E-mail: Lvwuyun_blue@163.com;

Cite this article: 

Lü Wu-yun, YANG Nan, XU Zhe, DAI Han, TANG Shuai, WANG Zheng-yi. 2020. FgHAT2 is involved in regulating vegetative growth, conidiation, DNA damage repair, DON production and virulence in Fusarium graminearum. Journal of Integrative Agriculture, 19(7): 1813-1824.

Ai X, Parthun M R. 2004. The nuclear Hat1p/Hat2p complex: A molecular link between type B histone acetyltransferases and chromatin assembly. Molecular Cell, 14, 195–205.
Barman H K, Takami Y, Ono T, Nishijima H, Sanematsu F, Shibahara K I, Nakayama T. 2006. Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochemical and Biophysical Reseach Communications, 345, 1547–1557.
Benson L J, Phillips J A, Gu Y, Parthun M R, Hoffman C S, Annunziato A T. 2007. Properties of the type B histone acetyltransferase Hat1. Journal of Biological Chemistry, 282, 836–842.
Berger S L, Kouzarides T, Shiekhattar R, Shilatifard A. 2009. An operational definition of epigenetics. Genes & Development, 23, 781.
Boltengagen M, Huang A, Boltengagen A, Trixl L, Lindner H, Kremser L, Offterdinger M, Lusser A. 2016. A novel role for the histone acetyltransferase Hat1 in the CENP-A/CID assembly pathway in Drosophila melanogaster. Nucleic Acids Research, 44, 2145–2159.
Brownell J E, Allis C D. 1996. Special HATs for special occasions: Linking histone acetylation to chromatin assembly and gene activation. Current Opinion in Genetics & Development, 6, 176–184.
Dawei Z, Huaxun Y, Hongqing G, Abbagail J, Meishan Z, Honghui L, Yin Y. 2014. Transcription factor HAT1 is phosphorylated by BIN2 kinase and mediates brassinosteroid repressed gene expression in Arabidopsis. The Plant Journal, 77, 59–70.
Feller C, Forné I, Imhof A, Becker P B. 2015. Global and specific responses of the histone acetylome to systematic perturbation. Molecular Cell, 57, 559–571.
Ge Z, Wang H, Parthun M R. 2011. Nuclear hat1p complex (NuB4) components participate in DNA repair-linked chromatin reassembly. Journal of Biological Chemistry, 286, 16790.
Han N, Shi L, Guo Q, Sun W, Yu Y, Yang L, Zhang X, Zhang M. 2017. HAT1 induces lung cancer cell apoptosis via up regulating Fas. Oncotarget, 8, 89970–89977.
Imhof A, Wolffe A P. 1999. Purification and properties of the Xenopus Hat1 acetyltransferase: Association with the 14-3-3 proteins in the oocyte nucleus. Biochemistry, 38, 13085–13093.
Jha P K, Khan M I, Mishra A, Das P, Sinha K K. 2017. HAT2 mediates histone H4K4 acetylation and affects micrococcal nuclease sensitivity of chromatin in Leishmania donovani. PLoS ONE, 12, e0177372.
Kelly T J, Qin S, Gottschling D E, Parthun M R. 2000. Type B histone acetyltransferase Hat1p participates in telomeric silencing. Molecular and Cellular Biology, 20, 7051–7058.
Kleff S, Andrulis E D, Anderson C W, Sternglanz R. 1995. Identification of a gene encoding a yeast histone H4 acetyltransferase. Journal of Biological Chemistry, 270, 24674–24677.
Kong X, van Diepeningen A D, Taj V D L, 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.
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.
Liu X, Jiang J, Yin Y, Ma Z. 2013. Involvement of FgERG4 in ergosterol biosynthesis, vegetative differentiation and virulence in Fusarium graminearum. Molecular Plant Pathology, 14, 71–83.
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.
Lv W, Wang C, Yang N, Que Y, Talbot N J, Wang Z. 2017. Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in Fusarium graminearum. Scientific Reports, 7, 11062.
Mirocha C J, Kolaczkowski E, Xie W, Yu H, Jelen H H. 1998. Analysis of deoxynivalenol and its derivatives (batch and single kernel) using gas chromatography/mass spectrometry. Journal of Agricultural and Food Chemistry, 46, 1414–1418.
Niehaus E M, Rindermann L, Janevska S, Münsterkötter M, Güldener U, Tudzynski B. 2018. Analysis of the global regulator Lae1 uncovers a connection between Lae1 and the histone acetyltransferase HAT1 in Fusarium fujikuroi. Applied Microbiology Biotechnology, 102, 279–295.
Parthun M R. 2007. Hat1: The emerging cellular roles of a type B histone acetyltransferase. Oncogene, 26, 5319–5328.
Parthun M R. 2012. Histone acetyltransferase 1: More than just an enzyme? Biochimica et Biophysica Acta (Gene Regulatory Mechanisms), 1819, 256–263.
Parthun M R, Widom J, Gottschling D E. 1996. The major cytoplasmic histone acetyltransferase in yeast: Links to chromatin replication and histone metabolism. Cell, 87, 85–94.
Poveda A, Pamblanco M, Tafrov S, Tordera V, Sternglanz R, Sendra R. 2004. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. Journal of Biological Chemistry, 279, 16033–16043.
Qian Y W, Lee E Y. 1995. Dual retinoblastoma-binding proteins with properties related to a negative regulator of Ras in yeast. Journal of Biological Chemistry, 270, 25507–25513.
Ruizgarcía A B, Sendra R, Galiana M, Pamblanco M, Pérezortín J E, Tordera V. 1998. HAT1 and HAT2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. Journal of Biological Chemistry, 273, 12599–12605.
Sobel R E, Cook R G, Perry C A, Annunziato A T, Allis C D. 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proceedings of the National Academy of Sciences of the United States of America, 92, 1237–1241.
Song Q, Parthun M R. 2002. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Molecular and Cellular Biology, 22, 8353–8365.
Struhl K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes & Development, 12, 599–606.
Sun H, Kennedy P J, Nestler E J. 2013. Epigenetics of the depressed brain: Role of histone acetylation and methylation. Neuropsychopharmacology, 38, 124–137.
Suter B, Pogoutse O, Guo X, Krogan N, Lewis P, Greenblatt J F, Rine J, Emili A. 2007. Association with the origin recognition complex suggests a novel role for histone acetyltransferase Hat1p/Hat2p. BMC Biology, 5, 38.
Tscherner M, Stappler E, Hnisz D, Kuchler K. 2012. The histone acetyltransferase Hat1 facilitates DNA damage repair and morphogenesis in Candida albicans. Molecular Microbiology, 86, 1197–1214.
Tscherner M, Zwolanek F, Jenull S, Sedlazeck F J, Petryshyn A, Frohner I E, Mavrianos J, Chauhan N, von Haeseler A, Kuchler K. 2015. The Candida albicans histone acetyltransferase Hat1 regulates stress resistance and virulence via distinct chromatin assembly pathways. PLoS Pathogens, 11, e1005218.
Verreault A, Kaufman P D, Kobayashi R, Stillman B. 1996. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell, 87, 95–104.
Yin Z, Chen C, Yang J, Feng W, Liu X, Zuo R, Wang J, Yang L, Zhong K, Gao C, Zhang H, Zheng X, Wang P, Zhang Z. 2019. Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae. Autophagy, 15, 1231–1257.
Yu J H, Hamari Z, Han K H, Seo J A, Reyesdomínguez Y, Scazzocchio C. 2004. Double-joint PCR: A PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genetics and Biology, 41, 973–981.
Zhang Q, Chen L, Yu X, Liu H, Akhberdi O, Pan J, Zhu X. 2016. A B-type histone acetyltransferase Hat1 regulates secondary metabolism, conidiation, and cell wall integrity in the taxol-producing fungus Pestalotiopsis microspora. Journal of Basic Microbiology, 56, 1380–1391.
[1] KANG Jin-bo, ZHANG Jie, LIU Yin-kai, SONG Ji-chang, OU Jian-lin, TAO Xian, ZHOU Ming-guo, DUAN Ya-bing. Mitochondrial dynamics caused by QoIs and SDHIs fungicides depended on FgDnm1 in Fusarium graminearum[J]. >Journal of Integrative Agriculture, 2023, 22(2): 481-494.
[2] LIU Na, LIAN Sen, ZHOU Shan-yue, WANG Cai-xia, REN Wei-chao, LI Bao-hua. Involvement of the autophagy-related gene BdATG8 in development and pathogenicity in Botryosphaeria dothidea[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2319-2328.
[3] CHEN A-hai, Tofazzal ISLAM, MA Zhong-hua. An integrated pest management program for managing fusarium head blight disease in cereals[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3434-3444.
[4] ZHANG Li-mei, CHEN Shu-ting, QI Min, CAO Xue-qi, LIANG Nan, LI Qian, TANG Wei, LU Guo-dong, ZHOU Jie, YU Wen-ying, WANG Zong-hua, ZHENG Hua-kun. The putative elongator complex protein Elp3 is involved in asexual development and pathogenicity by regulating autophagy in the rice blast fungus[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2944-2956.
[5] GONG Xiao-dong, LIU Yu-wei, BI Huan-huan, YANG Xiao-rong, HAN Jian-min, DONG Jin-gao, GU Shou-qin. StKU80, a component in the NHEJ repair pathway, is involved in mycelial morphogenesis, conidiation, appressorium development, and oxidative stress reactions in Exserohilum turcicum[J]. >Journal of Integrative Agriculture, 2021, 20(1): 147-158.
[6] PAN Li-jun, LU Lin, LIU Yu-ping, WEN Sheng-xian, ZHANG Zeng-yan. The M43 domain-containing metalloprotease RcMEP1 in Rhizoctonia cerealis is a pathogenicity factor during the fungus infection to wheat[J]. >Journal of Integrative Agriculture, 2020, 19(8): 2044-2055.
[7] 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.
[8] CHEN Bin, TIAN Yan-li, ZHAO Yu-qiang, WANG Jia-nan, XU Zhi-gang, LI Xiang, HU Bai-shi. Bleeding canker of pears caused by Dickeya fangzhongdai: Symptoms, etiology and biology[J]. >Journal of Integrative Agriculture, 2020, 19(4): 889-897.
[9] SONG Su-qin, Lü Zhuo, WANG Jing, ZHU Jing, GU Mei-ying, TANG Qi-yong, ZHANG Zhi-dong, WANG Wei, ZHANG Li-juan, WANG Bo. First report of a new potato disease caused by Galactomyces candidum F12 in China[J]. >Journal of Integrative Agriculture, 2020, 19(10): 2470-2476.
[10] WU Kai-li, CHEN Wei-zhong, YANG Shuai, WEN Ya, ZHENG Yu-ru, Wilfred Mabeche Anjago, YUN Ying-zi, WANG Zong-hua.
Isolation and identification of Fusarium oxysporum f. sp. cubense in Fujian Province, China
[J]. >Journal of Integrative Agriculture, 2019, 18(8): 1905-1913.
[11] CHANG Ji-tao, YU De-bin, LIANG Jian-bin, CHEN Jia, WANG Jian-fa, WANG Fang, JIANG Zhi-gang, HE Xi-jun, WU Rui, YU Li. Mycoplasma leachii causes bovine mastitis: Evidence from clinical symptoms, histopathology and immunohistochemistry[J]. >Journal of Integrative Agriculture, 2019, 18(1): 160-168.
[12] JIA Xiao-hui, FU Jun-fan, WANG Wen-hui, CUI Jian-chao, DU Yan-min, ZHOU Ru-jun, SUN Pingping. First report of Athelia bombacina causing postharvest fruit rot on pear[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2596-2599.
[13] WANG Li-min, ZHANG Yi-fan, DU Zhen-lin, Kang Rui-jiao, CHEN Lin-lin, XING Xiao-ping, YUAN Hong-xia, Ding Sheng-li, LI Hong-lian. FpPDE1 function of Fsarium pseudograminearum on pathogenesis in wheat[J]. >Journal of Integrative Agriculture, 2017, 16(11): 2504-2512.
[14] WEN Chu, ZHONG Qi, ZHANG Jia-dong, LU Jian-shan, ZHANG Li-xin, YUAN Xi-min, GAN Menghou, CAI Xue-peng, ZHANG Guo-zhong. Sequence and phylogenetic analysis of chicken reoviruses in China[J]. >Journal of Integrative Agriculture, 2016, 15(8): 1846-1855.
[15] HUANG Min, LIN Li, WU Yi-xin, Honhing Ho, HE Peng-fei, LI Guo-zhi, HE Peng-bo, XIONG Guo-ru, YUAN Yuan, HE Yue-qiu. Pathogenicity of Klebsiella pneumonia (KpC4) infecting maize and mice[J]. >Journal of Integrative Agriculture, 2016, 15(7): 1510-1520.
No Suggested Reading articles found!