Functional characterization of BbEaf6, a homolog of Eaf6 in Beauveria bassiana: Implications for fungal virulence and stress response

References

• Millar CB, Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol. 2006;7(9):657–666. doi: 10.1038/nrm1986
   PubMed Web of Science ®Google Scholar
• Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128(4):707–719. doi: 10.1016/j.cell.2007.01.015
   PubMed Web of Science ®Google Scholar
• Wang Z, Zang C, Cui K, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell. 2009;138(5):1019–1031. doi: 10.1016/j.cell.2009.06.049
   PubMed Web of Science ®Google Scholar
• Doyon Y, Selleck W, Lane WS, et al. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol. 2004;24(5):1884–1896. doi: 10.1128/MCB.24.5.1884-1896.2004
   PubMed Web of Science ®Google Scholar
• Keogh MC, Mennella TA, Sawa C, et al. The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev. 2006;20(5):660–665. doi: 10.1101/gad.1388106
   PubMedGoogle Scholar
• Doyon Y, Cote J. The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev. 2004;14(2):147–154. doi: 10.1016/j.gde.2004.02.009
   PubMed Web of Science ®Google Scholar
• Squatrito M, Gorrini C, Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 2006;16(8):433–442.
   PubMedGoogle Scholar
• Krogan NJ, Baetz K, Keogh MC, et al. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc Natl Acad Sci USA. 2004;101(37):13513–13518.
   PubMedGoogle Scholar
• Lin YY, Lu JY, Zhang J, et al. Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell. 2009;136(6):1073–1084. doi: 10.1016/j.cell.2009.01.033
   PubMed Web of Science ®Google Scholar
• Downey M, Knight B, Vashisht AA, et al. Acetylome profiling reveals overlap in the regulation of diverse processes by sirtuins, GCN5, and ESA1. Mol Cell Proteomics. 2015;14(1):162–176.
   PubMed Web of Science ®Google Scholar
• Taverna SD, Ilin S, Rogers RS, et al. 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. 2006;24(5):785–796. doi: 10.1016/j.molcel.2006.10.026
   PubMed Web of Science ®Google Scholar
• Wang X, Chang P, Ding J, Chen J. Architecture of the Saccharomyces cerevisiae NuA4/TIP60 complex. Nat Commun. 2018;9:1147.
   PubMed Web of Science ®Google Scholar
• Ullah M, Pelletier N, Xiao L, et al. Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol Cell Biol. 2008;28(20):6828–6843.
   PubMedGoogle Scholar
• Yang XJ. MOZ and MORF acetyltransferases: molecular interaction, animal development and human disease. Biochim Biophys Acta. 2015;1853(8):1818–1826. doi: 10.1016/j.bbamcr.2015.04.014
   PubMed Web of Science ®Google Scholar
• Mitchell L, Lambert JP, Gerdes M, et al. 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. 2008;28(7):2244–2256. doi: 10.1128/MCB.01653-07
   PubMedGoogle Scholar
• Lafon A, Chang CS, Scott EM, Jacobson SJ, Pillus L. MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene. 2007;26(38):5373–5384.
   PubMedGoogle Scholar
• Panagopoulos I, Micci F, Thorsen J, et al. Novel fusion of MYST/Esa1-associated factor 6 and PHF1 in endometrial stromal sarcoma. PLoS One. 2012;7(6):e39354. doi: 10.1371/journal.pone.0039354
   PubMed Web of Science ®Google Scholar
• Zhou JX, Su XM, Zheng SY, et al. The Arabidopsis NuA4 histone acetyltransferase complex is required for chlorophyll biosynthesis and photosynthesis. J Integr Plant Biol. 2022;64(4):901–914. doi: 10.1111/jipb.13227
   PubMedGoogle Scholar
• Kubo T, Yoshimura A, Kurata N Loss of OsEAF6, a Subunit of the Histone Acetyltransferase Complex, Causes Hybrid Breakdown in Intersubspecific Rice Crosses. Front Plant Sci. 2022;13:866404. 10.3389/fpls.2022.866404
   PubMedGoogle Scholar
• Qin J, Wu M, Zhou S FgEaf6 regulates virulence, asexual/sexual development and conidial septation in Fusarium graminearum. Curr Genet. 2020 Jun;66(3):517–529.10.1007/s00294-019-01043-0
   PubMedGoogle Scholar
• Mascarin GM, Jaronski ST. The production and uses of Beauveria bassiana as a microbial insecticide. World J Microbiol Biotechnol. 2016;32(11):177. doi: 10.1007/s11274-016-2131-3
   PubMed Web of Science ®Google Scholar
• Ortiz-Urquiza A, Luo ZB, Keyhani NO. Improving mycoinsecticides for insect biological control. Appl Microbiol Biotechnol. 2015;99(3):1057–1068. doi: 10.1007/s00253-014-6270-x
   PubMed Web of Science ®Google Scholar
• Ortiz-Urquiza A, Keyhani NO. Stress response signaling and virulence: insights from entomopathogenic fungi. Curr Genet. 2015;61(3):239–249. doi: 10.1007/s00294-014-0439-9
   PubMed Web of Science ®Google Scholar
• Xiao GH, Ying SH, Zheng P, et al. Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep. 2012;2(1):483. doi: 10.1038/srep00483
   PubMedGoogle Scholar
• Ortiz-Urquiza A, Keyhani NO. Molecular genetics of Beauveria bassiana infection of insects. Adv Genet. 2016;94:165249.
   Google Scholar
• Cai Q. Wang ZK, Shao W, et al. Essential role of Rpd3-dependent lysine modification in the growth, development and virulence of Beauveria bassiana. Environ Microbiol. 2018;20:1590–1606.
   PubMedGoogle Scholar
• Cai Q, Wang JJ, Fu B, Ying SH, Feng MG. Gcn5-dependent histone H3 acetylation and gene activity are required for the asexual development and virulence of Beauveria bassiana. Environ Microbiol. 2018;20:1484–1497.
   PubMed Web of Science ®Google Scholar
• Cai Q, Wang JJ, Shao W, et al. Rtt109-dependent histone H3 K56 acetylation and gene activity are essential for the biological control potential of Beauveria bassiana. Pest Manag Sci. 2018;74(11):2626–2635. doi: 10.1002/ps.5054
   PubMed Web of Science ®Google Scholar
• Cai Q, Wang JJ, Xie JT, Jiang DH, Keyhani NO. The Spt10 GNAT Superfamily Protein Modulates Development, Cell Cycle Progression and Virulence in the Fungal Insect Pathogen, Beauveria bassiana J Fungi (Basel). 2021;7(11):905.
   PubMedGoogle Scholar
• Cai Q, Wang J, Xie J, et al. The elongator subunit Elp3 regulates development, stress tolerance, cell cycle, and virulence in the entomopathogenic fungus beauveria bassiana. J Fungi (Basel). 2022;8(8):834. doi: 10.3390/jof8080834
   PubMedGoogle Scholar
• Wang JJ, Cai Q, Qiu L, et al. The histone acetyltransferase Mst2 sustains the biological control potential of a fungal insect pathogen through transcriptional regulation. Appl Microbiol Biotechnol. 2018;102(3):1343–1355. doi: 10.1007/s00253-017-8703-9
   PubMedGoogle Scholar
• Ying SH, Feng MG. Novel blastospore-based transformation system for easy integration of phosphinothricin resistance and green fluorescence protein genes into Beauveria bassiana. Appl Microbiol Biotechnol. 2006;72:206–210.
   PubMed Web of Science ®Google Scholar
• Chen J, Liu Q, Zeng L, et al. Protein Acetylation/Deacetylation: A Potential Strategy for Fungal Infection Control. Front Microbiol. 2020;11:574736. 10.3389/fmicb.2020.574736
   PubMedGoogle Scholar
• Wang X, Chang P, Ding J, Chen J. Distinct and redundant roles of the two MYST histone acetyltransferases Esa1 and Sas2 in cell growth and morphogenesis of Candida albicans. Eukaryot Cell. 2013;12:43–449.
   Google Scholar
• Chen X, Wu L, Lan H, et al. Histone acetyltransferases MystA and MystB contribute to morphogenesis and aflatoxin biosynthesis by regulating acetylation in fungus aspergillus flavus. Environ Microbiol. 2022;24(3):1340–1361. doi: 10.1111/1462-2920.15856
   PubMedGoogle Scholar
• O’Meara TR, Hay C, Price MS, et al. Cryptococcus neoformans histone acetyltransferase Gcn5 regulates fungal adaptation to the host. Eukaryot Cell. 2010;9(8):1193–1202. doi: 10.1128/EC.00098-10
   PubMedGoogle Scholar
• Kwon S, Lee J, Jeon J, et al. Role of the histone acetyltransferase Rtt109 in development and pathogenicity of the rice blast fungus. Mol Plant Microbe Interact. 2018;31(11):1200–1210. doi: 10.1094/MPMI-01-18-0015-R
   PubMed Web of Science ®Google Scholar
• González-Prieto JM, Rosas-Quijano R, Domínguez A, et al. The UmGcn5 gene encoding histone acetyltransferase from Ustilago maydis is involved in dimorphism and virulence. Fungal Genet Biol. 2014;71:86–95. 10.1016/j.fgb.2014.09.002
   PubMed Web of Science ®Google Scholar
• Qiu L, Wang JJ, Ying SH, et al. Wee1 and Cdc25 control morphogenesis, virulence and multistress tolerance of Beauveria bassiana by balancing cell cycle-required cyclin-dependent kinase 1 activity. Environ Microbiol. 2015;17(4):1119–1133. doi: 10.1111/1462-2920.12530
   PubMedGoogle Scholar
• Zhang AX, Mouhoumed AZ, Tong SM, et al. BrlA and AbaA Govern Virulence-Required Dimorphic Switch, Conidiation, and Pathogenicity in a Fungal Insect Pathogen. mSystems. 2019;4(4):e00140–19. doi: 10.1128/mSystems.00140-19
   PubMed Web of Science ®Google Scholar
• Guo CT, Luo XC, Ying SH, Feng MG. Differential Roles of Five Fluffy Genes (flbA-flbE) in the Lifecycle In Vitro and In Vivo of the Insect-Pathogenic Fungus Beauveria bassiana. J Fungi (Basel). 2022 Mar 23;8(4):334.
   PubMedGoogle Scholar
• Skelding KA, Rostas JA, Verrills NM. Controlling the cell cycle: the role of calcium/calmodulin-stimulated protein kinases I and II. Cell Cycle. 2011 Feb 15;10(4):631–9.
   PubMed Web of Science ®Google Scholar
• Bertoli C, Skotheim JM, de Bruin RA. Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol. 2013 Aug;14(8):518–28.
   PubMed Web of Science ®Google Scholar
• Tong SM, Chen Y, Zhu J, et al. Subcellular localization of five singular WSC domain-containing proteins and their roles in Beauveria bassiana responses to stress cues and metal ions. Environ Microbiol Rep. 2016 Apr;8(2):295–304.10.1111/1758-2229.12380
   PubMedGoogle Scholar
• Mou YN, Gao BJ, Ren K, et al. P-type Na+/K+ ATPases essential and nonessential for cellular homeostasis and insect pathogenicity of Beauveria bassiana. Virulence. 2020;11(1):1415–1431. doi: 10.1080/21505594.2020.1836903
   PubMed Web of Science ®Google Scholar
• Roy U, Kwon Y, Marie L, Symington L, Sung P, Lisby M, Greene EC. The Rad51 paralog complex Rad55-Rad57 acts as a molecular chaperone during homologous recombination. Mol Cell. 2021 Mar 4;81(5):1043–1057.e8.
   PubMedGoogle Scholar
• Gao BJ, Mou YN, Tong SM, et al. Subtilisin-like Pr1 proteases marking the evolution of pathogenicity in a wide-spectrum insect-pathogenic fungus. Virulence. 2020;11(1):365–380. doi: 10.1080/21505594.2020.1749487
   PubMed Web of Science ®Google Scholar
• Zhang SZ, Xia YX, Kim B, Keyhani NO. Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana Mol Microbiol. 2011;80:811–826.
   PubMedGoogle Scholar
• Cen K, Li B, Lu Y, et al. Divergent LysM effectors contribute to the virulence of Beauveria bassiana by evasion of insect immune defenses. PloS Pathog. 2017;13(9):e1006604. doi: 10.1371/journal.ppat.1006604
   PubMed Web of Science ®Google Scholar