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FgEaf6 regulates virulence, asexual/sexual development and conidial septation in Fusarium graminearum

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Abstract

Fusarium graminearum is a destructive fungal pathogen and a major cause of Fusarium head blight (FHB) which results in severe grain yield losses and quality reduction. Additionally, the pathogen produces mycotoxins during plant infection, which are harmful to the health of humans and livestock. As it is well known that lysine acetyltransferase complexes play important roles in pathogenesis, the roles of the Eaf6 homolog-containing complex have not been reported in fungal pathogen. In this study, a Eaf6 homolog FgEaf6 was identified in F. graminearum. To investigate the functions of FgEaf6, the gene was deleted using the split-marker method. ΔFgEaf6 mutant exhibited manifold defects in hyphal growth, conidial septation, asexual and sexual reproduction. Moreover, the virulence of the ΔFgEaf6 mutant was drastically reduced in both wheat heads and wheat coleoptiles. However, the FgEaf6 gene deletion did not impact DON production. An FgEaf6–gfp fusion localized to the nucleus and a conserved coiled-coil (C–C) domain was predicted in the sequence. Mutants with deletions in the C–C domain displayed similar defects during development and virulence as observed in the ΔFgEaf6 mutant. Moreover, the truncated gene was cytoplasm localized. In conclusion, the FgEaf6 encodes a nuclear protein, which plays key regulatory roles in hyphal growth, conidial septation, asexual/sexual reproduction, and the virulence of F. graminearum. The C–C is an indispensable domain in the gene. This is the first report on Eaf6 homolog functioning in virulence of fungal pathogen.

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References

  • Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, Pillus L, Workman JL, Cote J (1999) NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 18:51085119

    Article  Google Scholar 

  • Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle L (2007) RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol Plant Microb Interact 20:627–636

    Article  CAS  Google Scholar 

  • Boudreault AA, Cronier D, Selleck W, Lacoste N, Utley RT, Allard S, Savard J, Lane WS, Tan S, Cote J (2003) Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin. Gene Dev 17:1415–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cánovas D, Marcos AT, Gacek A, Ramos MS, 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(4):1175–1189

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cao S, He Y, Hao C, Xu Y, Zhang H, Wang C, Liu H, Xu JR (2017) RNA editing of the AMD1 gene is important for ascus maturation and ascospore discharge in Fusarium graminearum. Sci Rep 4617

  • Catlett NL, Lee B, Yoder OC, Turgeon BG (2003) Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl 50:9–11

    Google Scholar 

  • Cavinder B, Sikhakolli U, Fellows KM, Trail F (2012) Sexual development and ascospore discharge in Fusarium graminearum. J Vis Exp 61:e3895

    Google Scholar 

  • Chen CJ, Yu JJ, Bi CW, Zhang YN, Xu JQ, Wang JX, Zhou MG (2009) Mutations in a beta-tubulin confer resistance of Gibberella zeae to benzimidazole fungicides. Phytopatho 99(12):1403–1411

    Article  CAS  Google Scholar 

  • Chen A, Xie Q, Lin Y, Xu H, Shang W, Zhang J, Zhang D, Zheng W, Li G, Wang Z (2016) Septins are involved in nuclear division, morphogenesis and pathogenicity in Fusarium graminearum. Fungal Genet Biol 94:79–87

    Article  CAS  PubMed  Google Scholar 

  • 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. Nat Commnun 9:3429

    Article  CAS  Google Scholar 

  • 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. Curr Genet 65:153. https://doi.org/10.1007/s00294-018-0853-5

    Article  CAS  PubMed  Google Scholar 

  • Dichtl K, Helmschrott C, Dirr F, Wagener J (2012) Deciphering CWI signalling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant rho GTPases. Mol Microbiol 83(3):506–519

    Article  CAS  PubMed  Google Scholar 

  • Ding SL, Mehrabi R, Koten C, Kang ZS, Wei YD, Seong KY, Kistler HC, Xu JR (2009) Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot Cell 8:867–876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyon Y, Cote J (2004) The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev 14:147–154

    Article  CAS  PubMed  Google Scholar 

  • Gale LR, Ward TJ, Balmas V, Kistler HC (2007) Population subdivision of Fusarium graminearum sensu stricto in the upper Midwestern United States. Phytopathology 97:1434–1439

    Article  CAS  PubMed  Google Scholar 

  • Gardiner DM, Kazan K, Manners JM (2009) Novel genes of Fusarium graminearum that negatively regulate deoxynivalenol production and virulence. Mol Plant–Microbe Interact 22:1588–1600

    Article  CAS  PubMed  Google Scholar 

  • Gomes CJ, Harman MW, Centuori SM, Wolgemuth CW, Martinez JD (2018) Measuring DNA content in live cells by fluorescence microscopy. Cell Div 13:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez-Prieto JM, 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 Genet Biol 71:86–95

    Article  CAS  PubMed  Google Scholar 

  • Grant PA, Eberharter A, John S, Cook RG, Turner BM, Workman JL (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274:5895–5900

    Article  CAS  PubMed  Google Scholar 

  • Hou ZM, Xue CY, Peng YL, Katan T, Kistler HC, Xu JR (2002) A mitogen activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microb Interact 15:1119–1127

    Article  CAS  Google Scholar 

  • Hou R, Jiang C, Zheng Q, Wang CF, Xu JR (2015) The AreA transcription factor mediates the regulation of deoxynivalenol (DON) synthesis by ammonium and cyclic adenosine monophosphate (cAMP) signalling in Fusarium graminearum. Mol Plant Pathol 16:987–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howlett BJ, 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 Pathog 8:e1002724

    Article  CAS  Google Scholar 

  • Hu S, Zhou X, Gu X, Cao S, Wang C, Xu J (2014) The cAMP-PKA pathway regulates growth, sexual and asexual differentiation, and pathogenesis in Fusarium graminearum. Mol Plant Microb Interact 27:557–566

    Article  CAS  Google Scholar 

  • Jain R, Valiante V, Remme N, Docimo T, Heinekamp T, Hertweck C, Gershenzon J, Haas H, Brakhage AA (2011) The map kinase mpka controls CWI, oxidative stress response, gliotoxin production and iron adaptation in Aspergillus fumigatus. Mol Microbiol 82(1):39–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon J, Kwon S, Lee YH (2014) Histone acetylation in fungal pathogens of plants. Plant Pathol J 30:1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang J, Yun Y, Liu Y, Ma Z (2012) FgVELB is associated with vegetative differentiation, secondary metabolism and virulence in Fusarium graminearum. Fungal Genet Biol 49:653–662. https://doi.org/10.1016/j.fgb.2012.06.005

  • Jiang C, Zhang SJ, Zhang Q, Tao Y, Wang CF, Xu JR (2015) FgSKN7 and FgATF1 have overlapping functions in ascosporogenesis, pathogenesis and stress responses in Fusarium graminearum. Environ Microbiol 17:1245–1260

    Article  CAS  PubMed  Google Scholar 

  • Jiang C, Zhang CK, Wu CL, Sun PP, Hou R, Liu HQ, Wang CF, Xu JR (2016) TRI6 and TRI10 play different roles in the regulation of deoxynivalenol (DON) production by cAMP signalling in Fusarium graminearum. Environ Microbiol 18:3689–3701

    Article  CAS  PubMed  Google Scholar 

  • Kong X, van Diepeningen AD, van der Lee TAJ, 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. Front Microbiol 9:654

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evolut 33:1870-1874

  • Li CH, Melesse M, Zhang SJ, Hao CF, Wang CF, Zhang HC, Hall MC, Xu JR (2015) FgCDC14 regulates cytokinesis, morphogenesis, and pathogenesis in Fusarium graminearum. Mol Microbiol 98:770–786

    Article  CAS  PubMed  Google Scholar 

  • Li C, Zhang Y, Wang H, Chen L, Zhang J, Sun M, Xu JR, 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. Mol Plant Pathol 19(4):909–921

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yin YN, Wu JB, Jiang JH, Ma ZH (2010) Identification and characterization of carbendazim-resistant isolates of Gibberella zeae. Plant Dis 94:1137–1142

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T) (-Delta Delta C) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Zhang H, Qi L, Zhang S, Zhou X, Zhang Y, Xu JR (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 Phytol 204:943–954

    Article  CAS  PubMed  Google Scholar 

  • Lupas AN, Gruber M (2005) The structure of alpha-helical coiled coils. Adv Protein Chem 70:37–78

    Article  CAS  PubMed  Google Scholar 

  • Lv W, Wu J, Xu Z, Dai H, Ma Z, Wang Z (2019) The putative histone-like transcription factor fghltf1 is required for vegetative growth, sexual reproduction, and virulence in Fusarium graminearum. Curr Genet 65:981–994

    Article  CAS  PubMed  Google Scholar 

  • Lysoe E, Seong KY, Kistler HC (2011) The transcriptome of Fusarium graminearum during the infection of wheat. Mol Plant Microbe Interact 24:995–1000

    Article  PubMed  CAS  Google Scholar 

  • Mäntylä E, Salokas K, Oittinen M, Aho V, Mäntysaari P, Palmujoki L, Kalliolinna O, Ihalainen TO, Niskanen EA, Timonen J, Viiri K, Vihinen-Ranta M (2016) Promoter targeted histone acetylation of chromatinized 1 parvoviral genome is essential for infection progress. J Virol. https://doi.org/10.1128/JVI.03160-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Mason JM, Arndt KM (2004) Coiled coil domains: stability, specificity, and biological implications. ChemBioChem 5:170–176

    Article  CAS  PubMed  Google Scholar 

  • McMullen M, Bergstrom G, Wolf ED, Dill-Macky R, Hershman D, Shaner G, Sanford DV (2012) A unified effort to fight an enemy of wheat and barley: fusarium Head Blight. Plant Dis 96(12):1712–1728

    Article  PubMed  Google Scholar 

  • Mitchell L, Lambert JP, Gerdes M, Al-Madhoun AS, Skerjanc IS, Figeys D, Baetz K (2008) Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that eaf1 is essential for complex integrity. Mol Cell Biol 28(7):2244–2256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park A, Cho A, Seo J, Min K, Son H, Lee J, Choi G, Kim J, Lee Y (2012) Functional analyses of regulators of G protein signaling in Gibberella zeae. Fungal Genet Biol 49:511–520

    Article  CAS  PubMed  Google Scholar 

  • Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microb Interact 8:593–601

    Article  CAS  Google Scholar 

  • Ren J, Sang Y, Lu J, Yao YF (2017) Protein acetylation and its role in bacterial virulence. Trends Microbiol 25(9):768–779

    Article  CAS  PubMed  Google Scholar 

  • Rosler SM, Kramer K, Finkemeier I, Humpf HU, Tudzynski B (2016) The SAGA complex in the rice pathogen Fusarium fujikuroi: structure and functional characterization. Mol Microbiol 102:951–974

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, Patel DJ, Aitchison JD, Tackett AJ, Allis CD (2007) Yng1 phd finger binding to h3 trimethylated at k4 promotes nua3 hat activity at k14 of h3 and transcription at a subset of targeted orfs. Mol Cell 24(5):785–796

    Article  CAS  Google Scholar 

  • Ullah M, Pelletier N, Xiao L, Zhao SP, Wang K, Degerny C, Tahmasebi S, Cayrou C, Doyon Y, Goh SL, Champagne N, Cote J, Yang XJ (2008) Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol Cell Biol 28:6828–6843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valiante V (2017) The CWI signaling pathway and its involvement in secondary metabolite production. J Fungi 3:68

    Article  CAS  Google Scholar 

  • Wang CF, Zhang SJ, Hou R, Zhao ZT, Zheng Q, Xu QJ, Zheng DW, Wang GH, Liu HQ, Gao XL, Ma JW, Kistler HC, Kang ZS, Xu JR (2011) Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7:e1002460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang X, Zhang H, Lu Y, Huang H, Dong X, Chen J, Dong J, Yang X, Hang H, Jiang T (2012) Coiled-coil networking shapes cell molecular machinery. Mol Biol Cell 23(19):3911–3922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AM, Wuo MG, Arora PS (2015) Protein–protein interactions mediated by helical tertiary structure motifs. J Am Chem Soc 137:11622–11630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Q, Chen A, Zhang Y, Zhang C, Hu Y, Luo Z, Wang B, Yun Y, Zhou J, Li G, Wang Z (2019) ESCRT-III accessory proteins regulate fungal development and plant infection in Fusarium graminearum. Curr Genet 65:1041

    Article  CAS  PubMed  Google Scholar 

  • Xu JR, Staiger CJ, Hamer JE (1998) Inactivation of the mitogen activated protein kinase MPS1 in the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA 95:12713–12718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Wang M, Tang G, Ma Z, Shao W (2019) The endocytic cargo adaptor complex is required for cell-wall integrity via interacting with the sensor fgwsc2b in Fusarium graminearum. Curr Genet 65:1071–1080

    Article  CAS  PubMed  Google Scholar 

  • Yang X-J (2015) MOZ and MORF acetyltransferases: molecular interaction, animal development and human disease. Biochim Biophys Acta (BBA) 1853(8):1818–1826

    Article  CAS  Google Scholar 

  • Yi X, Cheng J, Jiang Z, Hu W, Bie T, Gao D, Li D, Wu R, Li Y, Chen S, Cheng X, Liu J, Zhang Y, Cheng S (2018) Genetic analysis of fusarium head blight resistance in CIMMYT bread wheat line C615 using traditional and conditional QTL mapping. Front Plant Sci 9:573

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu F, Gu Q, Yun Y, Yin Y, Xu J, Shim W, Ma Z (2014) The TOR signaling pathway regulates vegetative development and virulence in Fusarium graminearum. New Phytol 203:219–232

    Article  CAS  PubMed  Google Scholar 

  • Yuan S, Zhou M (2005) A major gene for resistance to carbendazim, in field isolates of Gibberella zeae. Can J Plant Path 27(1):58–63

    Article  CAS  Google Scholar 

  • Zhang Q, Akhberdi O, Wei D, Chen L, Liu H, Wang D, Hao X, Zhu X (2018) A MYST histone acetyltransferase modulates conidia development and secondary metabolism in Pestalotiopsis microspora, a taxol producer. Sci Rep 8(1):8199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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. Curr Genet. https://doi.org/10.1007/s00294019-00994-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Wang L, Liang Y, Yu J (2019b) FgPEX4 is involved in development, pathogenicity, and CWI in Fusarium graminearum. Curr Genet 65:747. https://doi.org/10.1007/s00294-018-0925-6

    Article  CAS  PubMed  Google Scholar 

  • Zheng Q, Hou R, Zhang J, Ma J, Wu Z, Wang G, Wang C, Xu JR (2013) The MAT locus genes play different roles in sexual reproduction and pathogenesis in Fusarium graminearum. PLoS ONE 8:e66980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou S, Wu C (2019) Comparative acetylome analysis reveals the potential roles of lysine acetylation for DON biosynthesis in Fusarium graminearum. BMC Genom. https://doi.org/10.1186/s12864-019-6227-7

    Article  Google Scholar 

  • Zhou XY, Heyer C, Choi YE, Mehrabi R, Xu JR (2010) The CID1 cyclin C-like gene is important for plant infection in Fusarium graminearum. Fungal Genet Biol 47:143–151

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the open project of the State Key Laboratory of Crop Stress Biology for Arid Areas (CSBAA2016001).

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  1. College of Plant Health and Medicine, The Key Lab of Integrated Crop Pests Management of Shandong Province, Qingdao Agricultural University, No. 700 Changcheng Road, Chengyang, Qingdao, 266109, Shandong, China

    Jiaxing Qin & Shanyue Zhou

  2. State Key Laboratory of Crop Stress Biology for Arid Aeras, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Mengchun Wu

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Qin, J., Wu, M. & Zhou, S. FgEaf6 regulates virulence, asexual/sexual development and conidial septation in Fusarium graminearum. Curr Genet 66, 517–529 (2020). https://doi.org/10.1007/s00294-019-01043-0

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