Effect of H2A.Z deletion is rescued by compensatory mutations in Fusarium graminearum
Autoři:
Zhenhui Chen aff001; Enric Zehraoui aff001; Anna K. Atanasoff-Kardjalieff aff002; Joseph Strauss aff002; Lena Studt aff002; Nadia Ponts aff001
Působiště autorů:
INRAE, MycSA, Villenave d’Ornon, France
aff001; Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, Austria
aff002
Vyšlo v časopise:
Effect of H2A.Z deletion is rescued by compensatory mutations in Fusarium graminearum. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009125
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009125
Souhrn
Fusarium head blight is a destructive disease of grains resulting in reduced yields and contamination of grains with mycotoxins worldwide; Fusarium graminearum is its major causal agent. Chromatin structure changes play key roles in regulating mycotoxin biosynthesis in filamentous fungi. Using a split-marker approach in three F. graminearum strains INRA156, INRA349 and INRA812 (PH-1), we knocked out the gene encoding H2A.Z, a ubiquitous histone variant reported to be involved in a diverse range of biological processes in yeast, plants and animals, but rarely studied in filamentous fungi. All ΔH2A.Z mutants exhibit defects in development including radial growth, sporulation, germination and sexual reproduction, but with varying degrees of severity between them. Heterogeneity of osmotic and oxidative stress response as well as mycotoxin production was observed in ΔH2A.Z strains. Adding-back wild-type H2A.Z in INRA349ΔH2A.Z could not rescue the phenotypes. Whole genome sequencing revealed that, although H2A.Z has been removed from the genome and the deletion cassette is inserted at H2A.Z locus only, mutations occur at other loci in each mutant regardless of the genetic background. Genes affected by these mutations encode proteins involved in chromatin remodeling, such as the helicase Swr1p or an essential subunit of the histone deacetylase Rpd3S, and one protein of unknown function. These observations suggest that H2A.Z and the genes affected by such mutations are part or the same genetic interaction network. Our results underline the genetic plasticity of F. graminearum facing detrimental gene perturbation. These findings suggest that intergenic suppressions rescue deleterious phenotypes in ΔH2A.Z strains, and that H2A.Z may be essential in F. graminearum. This assumption is further supported by the fact that H2A.Z deletion failed in another Fusarium spp., i.e., the rice pathogen Fusarium fujikuroi.
Zdroje
1. Balzer A, Tardieu D, Bailly J, Guerre P. The trichothecenes: Toxins nature, natural occurrence in food and feeds, and ways of struggle. Rev Med Veterinaire. 2004 Jun 1;155:299–314.
2. Goswami RS, Kistler HC. Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol. 2004 Nov 1;5(6):515–25. doi: 10.1111/j.1364-3703.2004.00252.x 20565626
3. Sutton JC. Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can J Plant Pathol. 1982 Jun 1;4(2):195–209.
4. McMullen M, Jones R, Gallenberg D. Scab of Wheat and Barley: A Re-emerging Disease of Devastating Impact. Plant Dis. 1997 Dec 1;81(12):1340–8. doi: 10.1094/PDIS.1997.81.12.1340 30861784
5. Desjardins AE, Hohn TM, McCormick SP. Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Rev. 1993;57(3):595–604. 8246841
6. Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M. Molecular and genetic studies of fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotechnol Biochem. 2007 Sep;71(9):2105–23. doi: 10.1271/bbb.70183 17827683
7. Figueroa M, Hammond-Kosack KE, Solomon PS. A review of wheat diseases—a field perspective. Mol Plant Pathol. 2018;19(6):1523–36. doi: 10.1111/mpp.12618 29045052
8. Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A. Structure of the nucleosome core particle at 7 Å resolution. Nature. 1984 Oct 11;311:532. doi: 10.1038/311532a0 6482966
9. Luger K, Dechassa ML, Tremethick DJ. New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat Rev Mol Cell Biol. 2012 Jun 22;13:436. doi: 10.1038/nrm3382 22722606
10. Audia JE, Campbell RM. Histone Modifications and Cancer. Cold Spring Harb Perspect Biol [Internet]. 2016 Apr [cited 2019 Aug 12];8(4). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4817802/ doi: 10.1101/cshperspect.a019521 27037415
11. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Mol Biol. 2003 Nov;10(11):882–91. doi: 10.1038/nsb996 14583738
12. Bonisch C, Hake SB. Histone H2A variants in nucleosomes and chromatin: more or less stable? Nucleic Acids Res. 2012 Nov 1;40(21):10719–41. doi: 10.1093/nar/gks865 23002134
13. Bernstein E, Hake SB. The nucleosome: a little variation goes a long wayThis paper is one of a selection of papers published in this Special Issue, entitled 27th International West Coast Chromatin and Chromosome Conference, and has undergone the Journal’s usual peer review process. Biochem Cell Biol. 2006 Aug;84(4):505–7. doi: 10.1139/o06-085 16936823
14. van Daal A, White EM, Elgin SC, Gorovsky MA. Conservation of intron position indicates separation of major and variant H2As is an early event in the evolution of eukaryotes. J Mol Evol. 1990 May;30(5):449–55. doi: 10.1007/BF02101116 2111857
15. Thatcher TH, Gorovsky MA. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res. 1994 Jan 25;22(2):174–9. doi: 10.1093/nar/22.2.174 8121801
16. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 1997 Sep;389(6648):251–60. doi: 10.1038/38444 9305837
17. Suto RK, Clarkson MJ, Tremethick DJ, Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol. 2000 Dec;7(12):1121–4. doi: 10.1038/81971 11101893
18. March-Díaz R, Reyes JC. The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant. 2009 Jul;2(4):565–77. doi: 10.1093/mp/ssp019 19825639
19. Jackson JD, Falciano VT, Gorovsky MA. A likely histone H2A.F/Z variant in Saccharomyces cerevisiae. Trends Biochem Sci. 1996 Dec;21(12):466–7. doi: 10.1016/s0968-0004(96)20028-3 9009827
20. van Daal A, Elgin SC. A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell. 1992 Jun;3(6):593–602. doi: 10.1091/mbc.3.6.593 1498368
21. Hatch CL, Bonner WM. The human histone H2A.Z gene. Sequence and regulation. J Biol Chem. 1990 Sep 5;265(25):15211–8. 1697587
22. Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N, et al. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell. 2004 Dec 22;16(6):979–90. doi: 10.1016/j.molcel.2004.12.003 15610740
23. Keogh M-C, Kim J-A, Downey M, Fillingham J, Chowdhury D, Harrison JC, et al. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature. 2006 Jan 26;439(7075):497–501. doi: 10.1038/nature04384 16299494
24. Krogan NJ, Peng W-T, Cagney G, Robinson MD, Haw R, Zhong G, et al. High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell. 2004 Jan 30;13(2):225–39. doi: 10.1016/s1097-2765(04)00003-6 14759368
25. Kalocsay M, Hiller NJ, Jentsch S. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell. 2009 Feb 13;33(3):335–43. doi: 10.1016/j.molcel.2009.01.016 19217407
26. Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD. Histone H2A.Z Controls a Critical Chromatin Remodeling Step Required for DNA Double-Strand Break Repair. Mol Cell. 2012 Dec 14;48(5):723–33. doi: 10.1016/j.molcel.2012.09.026 23122415
27. Gursoy-Yuzugullu O, Ayrapetov MK, Price BD. Histone chaperone Anp32e removes H2A.Z from DNA double-strand breaks and promotes nucleosome reorganization and DNA repair. Proc Natl Acad Sci. 2015 Jun 16;112(24):7507–12. doi: 10.1073/pnas.1504868112 26034280
28. Alatwi HE, Downs JA. Removal of H2A.Z by INO80 promotes homologous recombination. EMBO Rep. 2015 Aug 1;16(8):986–94. doi: 10.15252/embr.201540330 26142279
29. Marques JT, Kim K, Wu P-H, Alleyne TM, Jafari N, Carthew RW. Loqs and R2D2 act sequentially in the siRNA pathway in Drosophila. Nat Struct Mol Biol. 2010 Jan;17(1):24–30. doi: 10.1038/nsmb.1735 20037596
30. Deal RB, Henikoff S. The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat Protoc. 2011 Jan;6(1):56–68. doi: 10.1038/nprot.2010.175 21212783
31. Soboleva TA, Nekrasov M, Ryan DP, Tremethick DJ. Histone variants at the transcription start-site. Trends Genet. 2014 May 1;30(5):199–209. doi: 10.1016/j.tig.2014.03.002 24768041
32. Faast R, Thonglairoam V, Schulz TC, Beall J, Wells JR, Taylor H, et al. Histone variant H2A.Z is required for early mammalian development. Curr Biol CB. 2001 Aug 7;11(15):1183–7. doi: 10.1016/s0960-9822(01)00329-3 11516949
33. Iouzalen N, Moreau J, Méchali M. H2A.ZI, a new variant histone expressed during Xenopus early development exhibits several distinct features from the core histone H2A. Nucleic Acids Res. 1996 Oct 15;24(20):3947–52. doi: 10.1093/nar/24.20.3947 8918796
34. Liu X, Li B, GorovskyMA null. Essential and nonessential histone H2A variants in Tetrahymena thermophila. Mol Cell Biol. 1996 Aug;16(8):4305–11. doi: 10.1128/mcb.16.8.4305 8754831
35. Adam M, Robert F, Larochelle M, Gaudreau L. H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol. 2001 Sep;21(18):6270–9. doi: 10.1128/mcb.21.18.6270-6279.2001 11509669
36. Jackson JD, Gorovsky MA. Histone H2A.Z has a conserved function that is distinct from that of the major H2A sequence variants. Nucleic Acids Res. 2000 Oct 1;28(19):3811–6. doi: 10.1093/nar/28.19.3811 11000274
37. van Attikum H, Fritsch O, Gasser SM. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 2007 Sep 19;26(18):4113–25. doi: 10.1038/sj.emboj.7601835 17762868
38. Gerhold CB, Gasser SM. INO80 and SWR complexes: relating structure to function in chromatin remodeling. Trends Cell Biol. 2014 Nov;24(11):619–31. doi: 10.1016/j.tcb.2014.06.004 25088669
39. Morrison AJ, Shen X. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat Rev Mol Cell Biol. 2009 Jun;10(6):373–84. doi: 10.1038/nrm2693 19424290
40. Tosi A, Haas C, Herzog F, Gilmozzi A, Berninghausen O, Ungewickell C, et al. Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell. 2013 Sep 12;154(6):1207–19. doi: 10.1016/j.cell.2013.08.016 24034245
41. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273–304. doi: 10.1146/annurev.biochem.77.062706.153223 19355820
42. Chen M, Licon K, Otsuka R, Pillus L, Ideker T. Decoupling epigenetic and genetic effects through systematic analysis of gene position. Cell Rep. 2013 Jan 31;3(1):128–37. doi: 10.1016/j.celrep.2012.12.003 23291096
43. Chen Z, Ponts N. H2A.Z and chromatin remodelling complexes: a focus on fungi. Crit Rev Microbiol. 2020 May;46(3):321–37. doi: 10.1080/1040841X.2020.1781784 32594818
44. Ku M, Jaffe JD, Koche RP, Rheinbay E, Endoh M, Koseki H, et al. H2A.Z landscapes and dual modifications in pluripotent and multipotent stem cells underlie complex genome regulatory functions. Genome Biol. 2012 Oct 3;13(10):R85. doi: 10.1186/gb-2012-13-10-r85 23034477
45. Kumar SV. H2A.Z at the Core of Transcriptional Regulation in Plants. Mol Plant. 2018 Sep;11(9):1112–4. doi: 10.1016/j.molp.2018.07.002 30053606
46. Ryan DP, Tremethick DJ. The interplay between H2A.Z and H3K9 methylation in regulating HP1α binding to linker histone-containing chromatin. Nucleic Acids Res. 2018 Oct 12;46(18):9353–66. doi: 10.1093/nar/gky632 30007360
47. Creyghton MP, Markoulaki S, Levine SS, Hanna J, Lodato MA, Sha K, et al. H2AZ Is Enriched at Polycomb Complex Target Genes in ES Cells and Is Necessary for Lineage Commitment. Cell. 2008 Nov 14;135(4):649–61. doi: 10.1016/j.cell.2008.09.056 18992931
48. Liu Y, Liu N, Yin Y, Chen Y, Jiang J, Ma Z. Histone H3K4 methylation regulates hyphal growth, secondary metabolism and multiple stress responses in Fusarium graminearum. Environ Microbiol. 2015 Nov;17(11):4615–30. doi: 10.1111/1462-2920.12993 26234386
49. Studt L, Janevska S, Arndt B, Boedi S, Sulyok M, Humpf H-U, et al. Lack of the COMPASS Component Ccl1 Reduces H3K4 Trimethylation Levels and Affects Transcription of Secondary Metabolite Genes in Two Plant–Pathogenic Fusarium Species. Front Microbiol [Internet]. 2017 [cited 2020 Jul 31];7. Available from: doi: 10.3389/fmicb.2016.02144 28119673
50. Bachleitner S, Sørensen JL, Gacek-Matthews A, Sulyok M, Studt L, Strauss J. Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism. Front Microbiol [Internet]. 2019 [cited 2019 Nov 15];10. Available from: https://www.frontiersin.org/articles/10.3389/fmicb.2019.01759/full#h4 31456754
51. Connolly LR, Smith KM, Freitag M. The Fusarium graminearum Histone H3 K27 Methyltransferase KMT6 Regulates Development and Expression of Secondary Metabolite Gene Clusters. Madhani HD, editor. PLoS Genet. 2013 Oct 31;9(10):e1003916. doi: 10.1371/journal.pgen.1003916 24204317
52. Dong Q, Wang Y, Qi S, Gai K, He Q, Wang Y. Histone variant H2A.Z antagonizes the positive effect of the transcriptional activator CPC1 to regulate catalase-3 expression under normal and oxidative stress conditions. Free Radic Biol Med. 2018 Jun 1;121:136–48. doi: 10.1016/j.freeradbiomed.2018.05.003 29738831
53. Cui G, Dong Q, Duan J, Zhang C, Liu X, He Q. NC2 complex is a key factor for the activation of catalase-3 transcription by regulating H2A.Z deposition. Nucleic Acids Res [Internet]. 2020 [cited 2020 Jul 31]; Available from: doi: 10.1093/nar/gkaa552 32633757
54. Courtney AJ, Kamei M, Ferraro AR, Gai K, He Q, Honda S, et al. Normal Patterns of Histone H3K27 Methylation Require the Histone Variant H2A.Z in Neurospora crassa. Genetics. 2020 Jul 10; doi: 10.1534/genetics.120.303442 32651262
55. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–402. doi: 10.1093/nar/25.17.3389 9254694
56. Liu H, Wang Q, He Y, Chen L, Hao C, Jiang C, et al. Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes. Genome Res. 2016 Apr;26(4):499–509. doi: 10.1101/gr.199877.115 26934920
57. Bui D-C, Lee Y, Lim JY, Fu M, Kim J-C, Choi GJ, et al. Heat shock protein 90 is required for sexual and asexual development, virulence, and heat shock response in Fusarium graminearum. Sci Rep. 2016 16;6:28154. doi: 10.1038/srep28154 27306495
58. Zhao C, Waalwijk C, de Wit PJGM, Tang D, van der Lee T. Relocation of genes generates non-conserved chromosomal segments in Fusarium graminearum that show distinct and co-regulated gene expression patterns. BMC Genomics. 2014 Mar 13;15:191. doi: 10.1186/1471-2164-15-191 24625133
59. Hays SM, Swanson J, Selker EU. Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa. Genetics. 2002 Mar;160(3):961–73. 11901114
60. May GS, Morris NR. The unique histone H2A gene of Aspergillus nidulans contains three introns. Gene. 1987;58(1):59–66. doi: 10.1016/0378-1119(87)90029-1 3319784
61. Kurat CF, Recht J, Radovani E, Durbic T, Andrews B, Fillingham J. Regulation of histone gene transcription in yeast. Cell Mol Life Sci CMLS. 2014 Feb;71(4):599–613. doi: 10.1007/s00018-013-1443-9 23974242
62. Merhej J, Urban M, Dufresne M, Hammond-Kosack KE, Richard-Forget F, Barreau C. The velvet gene, FgVe1, affects fungal development and positively regulates trichothecene biosynthesis and pathogenicity in Fusarium graminearum. Mol Plant Pathol. 2012 May;13(4):363–74. doi: 10.1111/j.1364-3703.2011.00755.x 22013911
63. Ponts N, Pinson-Gadais L, Verdal-Bonnin M-N, Barreau C, Richard-Forget F. Accumulation of deoxynivalenol and its 15-acetylated form is significantly modulated by oxidative stress in liquid cultures of Fusarium graminearum: DON-ADON accumulation is modulated by oxidative stress. FEMS Microbiol Lett. 2006 May;258(1):102–7. doi: 10.1111/j.1574-6968.2006.00200.x 16630263
64. Liu X, Dang Y, Matsu-Ura T, He Y, He Q, Hong CI, et al. DNA Replication Is Required for Circadian Clock Function by Regulating Rhythmic Nucleosome Composition. Mol Cell. 2017 Jul 20;67(2):203–213.e4. doi: 10.1016/j.molcel.2017.05.029 28648778
65. Kim H-S, Vanoosthuyse V, Fillingham J, Roguev A, Watt S, Kislinger T, et al. An acetylated form of histone H2A.Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat Struct Mol Biol. 2009 Dec;16(12):1286–93. doi: 10.1038/nsmb.1688 19915592
66. Ponts N. Mycotoxins are a component of Fusarium graminearum stress-response system. Front Microbiol [Internet]. 2015 Nov 4 [cited 2019 Aug 1];6. Available from: http://journal.frontiersin.org/Article/10.3389/fmicb.2015.01234/abstract 26583017
67. Seong K-Y, Pasquali M, Zhou X, Song J, Hilburn K, McCormick S, et al. Global gene regulation by Fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Mol Microbiol. 2009 Apr;72(2):354–67. doi: 10.1111/j.1365-2958.2009.06649.x 19320833
68. Davis BH, Poon AFY, Whitlock MC. Compensatory mutations are repeatable and clustered within proteins. Proc R Soc B Biol Sci. 2009 May 22;276(1663):1823–7. doi: 10.1098/rspb.2008.1846 19324785
69. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017 04;45(D1):D200–3. doi: 10.1093/nar/gkw1129 27899674
70. Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2020 Jan 8;48(D1):D265–8. doi: 10.1093/nar/gkz991 31777944
71. Wagner EJ, Carpenter PB. Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol. 2012 Feb;13(2):115–26. doi: 10.1038/nrm3274 22266761
72. Woo H, Ha SD, Lee SB, Buratowski S, Kim T. Modulation of gene expression dynamics by co-transcriptional histone methylations. Exp Mol Med. 2017 Apr;49(4):e326–e326. doi: 10.1038/emm.2017.19 28450734
73. Bošković A, Bender A, Gall L, Ziegler-Birling C, Beaujean N, Torres-Padilla M-E. Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation. Epigenetics. 2012 Jul 1;7(7):747–57. doi: 10.4161/epi.20584 22647320
74. Liao S-M, Du Q-S, Meng J-Z, Pang Z-W, Huang R-B. The multiple roles of histidine in protein interactions. Chem Cent J. 2013 Mar 1;7:44. doi: 10.1186/1752-153X-7-44 23452343
75. Morris AL, MacArthur MW, Hutchinson EG, Thornton JM. Stereochemical quality of protein structure coordinates. Proteins Struct Funct Bioinforma. 1992;12(4):345–64. doi: 10.1002/prot.340120407 1579569
76. Filteau M, Hamel V, Pouliot M-C, Gagnon-Arsenault I, Dubé AK, Landry CR. Evolutionary rescue by compensatory mutations is constrained by genomic and environmental backgrounds. Mol Syst Biol [Internet]. 2015 Oct 12 [cited 2019 Aug 9];11(10). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4631203/ doi: 10.15252/msb.20156444 26459777
77. Laurent B, Moinard M, Spataro C, Ponts N, Barreau C, Foulongne-Oriol M. Landscape of genomic diversity and host adaptation in Fusarium graminearum. BMC Genomics. 2017 23;18(1):203. doi: 10.1186/s12864-017-3524-x 28231761
78. Cuomo CA, Güldener U, Xu J-R, Trail F, Turgeon BG, Di Pietro A, et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science. 2007 Sep 7;317(5843):1400–2. doi: 10.1126/science.1143708 17823352
79. King R, Urban M, Hammond-Kosack MCU, Hassani-Pak K, Hammond-Kosack KE. The completed genome sequence of the pathogenic ascomycete fungus Fusarium graminearum. BMC Genomics. 2015 Jul 22;16:544. doi: 10.1186/s12864-015-1756-1 26198851
80. King R, Urban M, Hammond-Kosack KE. Annotation of Fusarium graminearum (PH-1) Version 5.0. Genome Announc. 2017 Jan 12;5(2). doi: 10.1128/genomeA.01479-16 28082505
81. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, et al. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res. 2012 Jan;40(Database issue):D675–681. doi: 10.1093/nar/gkr918 22064857
82. Basenko EY, Pulman JA, Shanmugasundram A, Harb OS, Crouch K, Starns D, et al. FungiDB: An Integrated Bioinformatic Resource for Fungi and Oomycetes. J Fungi. 2018 Mar;4(1):39. doi: 10.3390/jof4010039 30152809
83. Ruan K, Yamamoto TG, Asakawa H, Chikashige Y, Kimura H, Masukata H, et al. Histone H4 acetylation required for chromatin decompaction during DNA replication. Sci Rep. 2015 Jul 30;5:12720. doi: 10.1038/srep12720 26223950
84. Hanes SD. Prolyl isomerases in gene transcription. Biochim Biophys Acta. 2015 Oct;1850(10):2017–34. doi: 10.1016/j.bbagen.2014.10.028 25450176
85. Nelson CJ, Santos-Rosa H, Kouzarides T. Proline Isomerization of Histone H3 Regulates Lysine Methylation and Gene Expression. Cell. 2006 Sep 8;126(5):905–16. doi: 10.1016/j.cell.2006.07.026 16959570
86. Zhang Y, Shan C-M, Wang J, Bao K, Tong L, Jia S. Molecular basis for the role of oncogenic histone mutations in modulating H3K36 methylation. Sci Rep. 2017 03;7:43906. doi: 10.1038/srep43906 28256625
87. Rogawski DS, Ndoj J, Cho HJ, Maillard I, Grembecka J, Cierpicki T. Two Loops Undergoing Concerted Dynamics Regulate the Activity of the ASH1L Histone Methyltransferase. Biochemistry. 2015 Sep 8;54(35):5401–13. doi: 10.1021/acs.biochem.5b00697 26292256
88. Kavanagh KL, Jörnvall H, Persson B, Oppermann U. Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci CMLS. 2008 Dec;65(24):3895–906. doi: 10.1007/s00018-008-8588-y 19011750
89. Persson B, Kallberg Y, Oppermann U, Jörnvall H. Coenzyme-based functional assignments of short-chain dehydrogenases/reductases (SDRs). Chem Biol Interact. 2003 Feb 1;143–144:271–8. doi: 10.1016/s0009-2797(02)00223-5 12604213
90. Oppermann U, Filling C, Hult M, Shafqat N, Wu X, Lindh M, et al. Short-chain dehydrogenases/reductases (SDR): the 2002 update. Chem Biol Interact. 2003 Feb 1;143–144:247–53. doi: 10.1016/s0009-2797(02)00164-3 12604210
91. Kleiger G, Eisenberg D. GXXXG and GXXXA motifs stabilize FAD and NAD(P)-binding Rossmann folds through C(alpha)-H… O hydrogen bonds and van der waals interactions. J Mol Biol. 2002 Oct 11;323(1):69–76. doi: 10.1016/s0022-2836(02)00885-9 12368099
92. Wang Q, Jiang C, Wang C, Chen C, Xu J-R, Liu H. Characterization of the Two-Speed Subgenomes of Fusarium graminearum Reveals the Fast-Speed Subgenome Specialized for Adaption and Infection. Front Plant Sci. 2017;8:140. doi: 10.3389/fpls.2017.00140 28261228
93. Secombe J, Eisenman RN. The function and regulation of the JARID1 family of histone H3 lysine 4 demethylases: the Myc connection. Cell Cycle Georget Tex. 2007 Jun 1;6(11):1324–8. doi: 10.4161/cc.6.11.4269 17568193
94. Horton JR, Engstrom A, Zoeller EL, Liu X, Shanks JR, Zhang X, et al. Characterization of a Linked Jumonji Domain of the KDM5/JARID1 Family of Histone H3 Lysine 4 Demethylases. J Biol Chem. 2016 Feb 5;291(6):2631–46. doi: 10.1074/jbc.M115.698449 26645689
95. Gacek-Matthews A, Berger H, Sasaki T, Wittstein K, Gruber C, Lewis ZA, et al. KdmB, a Jumonji Histone H3 Demethylase, Regulates Genome-Wide H3K4 Trimethylation and Is Required for Normal Induction of Secondary Metabolism in Aspergillus nidulans. PLOS Genet. 2016 Aug 22;12(8):e1006222. doi: 10.1371/journal.pgen.1006222 27548260
96. Janevska S, Güldener U, Sulyok M, Tudzynski B, Studt L. Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation-specific transcription factor gene ABA1 in Fusarium fujikuroi. Environ Microbiol. 2018;20(9):3343–62. doi: 10.1111/1462-2920.14339 30047187
97. Wiemann P, Sieber CMK, von Bargen KW, Studt L, Niehaus EM, Espino JJ, et al. Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog. 2013;9(6):e1003475. doi: 10.1371/journal.ppat.1003475 23825955
98. Bömke C, Tudzynski B. Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry. 2009 Oct 1;70(15):1876–93.
99. Yu C, Zavaljevski N, Desai V, Reifman J. QuartetS: A fast and accurate algorithm for large-scale orthology detection [Internet]. Vol. 39, Nucleic Acids Research. 2011 [cited 2020 May 18]. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3141274/ doi: 10.1093/nar/gkr308 21572104
100. Teng X, Dayhoff-Brannigan M, Cheng W-C, Gilbert CE, Sing CN, Diny NL, et al. Genome-wide consequences of deleting any single gene. Mol Cell. 2013 Nov 21;52(4):485–94. doi: 10.1016/j.molcel.2013.09.026 24211263
101. Rojas Echenique JI, Kryazhimskiy S, Nguyen Ba AN, Desai MM. Modular epistasis and the compensatory evolution of gene deletion mutants. Butler G, editor. PLOS Genet. 2019 Feb 15;15(2):e1007958. doi: 10.1371/journal.pgen.1007958 30768593
102. Li X, Fan Z, Yan M, Qu J, Xu J-R, Jin Q. Spontaneous mutations in FgSAD1 suppress the growth defect of the Fgprp4 mutant by affecting tri-snRNP stability and its docking in Fusarium graminearum. Environ Microbiol. 2019;21(12):4488–503. doi: 10.1111/1462-2920.14736 31291045
103. Ilgen P, Hadeler B, Maier FJ, Schäfer W. Developing kernel and rachis node induce the trichothecene pathway of Fusarium graminearum during wheat head infection. Mol Plant-Microbe Interact MPMI. 2009 Aug;22(8):899–908. doi: 10.1094/MPMI-22-8-0899 19589066
104. Cappellini RA, Peterson JL. Macroconidium Formation in Submerged Cultures by a Non-Sporulating Strain of Gibberella zeae. Mycologia. 1965;57(6):962–6.
105. Boutigny A-L, Barreau C, Atanasova-Penichon V, Verdal-Bonnin M-N, Pinson-Gadais L, Richard-Forget F. Ferulic acid, an efficient inhibitor of type B trichothecene biosynthesis and Tri gene expression in Fusarium liquid cultures. Mycol Res. 2009 Jun 1;113(6):746–53. doi: 10.1016/j.mycres.2009.02.010 19249362
106. Darken MA, Jensen AL, Shu P. Production of gibberellic acid by fermentation. Appl Microbiol. 1959;7(12):301–3. 13814121
107. Geissman TA, Verbiscar AJ, Phinney BO, Cragg G. Studies on the biosynthesis of gibberellins from (-)-kaurenoic acid in cultures of Gibberella Fujikuroi. Phytochemistry. 1966;5(5):933–47.
108. Pontecorvo G, Roper JA, Chemmons LM, Macdonald KD, Bufton AWJ. The Genetics of Aspergillus nidulans. Adv Genet. 1953; doi: 10.1016/s0065-2660(08)60408-3 13040135
109. Schumacher J. Tools for Botrytis cinerea: New expression vectors make the gray mold fungus more accessible to cell biology approaches. Fungal Genet Biol. 2012;49(6):483–97. doi: 10.1016/j.fgb.2012.03.005 22503771
110. Ponts N, Yang J, Chung D-WD, Prudhomme J, Girke T, Horrocks P, et al. Deciphering the ubiquitin-mediated pathway in apicomplexan parasites: a potential strategy to interfere with parasite virulence. PloS One. 2008 Jun 11;3(6):e2386. doi: 10.1371/journal.pone.0002386 18545708
111. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, et al. Protein database searches using compositionally adjusted substitution matrices. FEBS J. 2005 Oct;272(20):5101–9. doi: 10.1111/j.1742-4658.2005.04945.x 16218944
112. Catlett N, Lee B-N, Yoder O, Turgeon B. Split-Marker Recombination for Efficient Targeted Deletion of Fungal Genes. Fungal Genet Rep. 2003 Dec 1;50(1):9–11.
113. Montibus M, Ducos C, Bonnin-Verdal M-N, Bormann J, Ponts N, Richard-Forget F, et al. The bZIP Transcription Factor Fgap1 Mediates Oxidative Stress Response and Trichothecene Biosynthesis But Not Virulence in Fusarium graminearum. Lee Y-W, editor. PLoS ONE. 2013 Dec 12;8(12):e83377. doi: 10.1371/journal.pone.0083377 24349499
114. Collopy PD, Colot HV, Park G, Ringelberg C, Crew CM, Borkovich KA, et al. High-throughput construction of gene deletion cassettes for generation of Neurospora crassa knockout strains. Methods Mol Biol Clifton NJ. 2010;638:33–40. doi: 10.1007/978-1-60761-611-5_3 20238259
115. Colot H V., Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci. 2006;103(27):10352–7. doi: 10.1073/pnas.0601456103 16801547
116. Staben C, Jensen B, Singer M, Pollock J, Schechtman M, Kinsey J, et al. Use of a bacterial hygromycin B resistance gene as a dominant selectable marker in Neurospora crassa transformation. Fungal Genet Rep. 2017;
117. Niehaus E-M, Münsterkötter M, Proctor RH, Brown DW, Sharon A, Idan Y, et al. Comparative “Omics” of the Fusarium fujikuroi Species Complex Highlights Differences in Genetic Potential and Metabolite Synthesis. Genome Biol Evol. 2016 Dec 31;8(11):3574–99. doi: 10.1093/gbe/evw259 28040774
118. Tudzynski B, Homann V, Feng B, Marzluf G a. Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Mol Gen Genet MGG. 1999;261:106–14. doi: 10.1007/s004380050947 10071216
119. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012 Jul;9(7):671–5. doi: 10.1038/nmeth.2089 22930834
120. Cavinder B, Sikhakolli U, Fellows KM, Trail F. Sexual Development and Ascospore Discharge in Fusarium graminearum. J Vis Exp JoVE [Internet]. 2012 Mar 29 [cited 2019 Aug 27];(61). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3460587/ doi: 10.3791/3895 22491175
121. Javerzat JP, Bhattacherjee V, Barreau C. Isolation of telomeric DNA from the filamentous fungus Podospora anserina and construction of a self-replicating linear plasmid showing high transformation frequency. Nucleic Acids Res. 1993 Feb 11;21(3):497–504. doi: 10.1093/nar/21.3.497 8441663
122. Bolger A, Scossa F, Bolger ME, Lanz C, Maumus F, Tohge T, et al. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat Genet. 2014 Sep;46(9):1034–8. doi: 10.1038/ng.3046 25064008
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