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Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum


Autoři: Hang Jiang aff001;  Aliang Xia aff001;  Meng Ye aff001;  Jingyi Ren aff001;  Dongao Li aff001;  Huiquan Liu aff001;  Qinhu Wang aff001;  Ping Lu aff001;  Chunlan Wu aff001;  Jin-Rong Xu aff002;  Cong Jiang aff001
Působiště autorů: State Key Laboratory of Crop Stress Biology for Arid Areas and NWAFU-Purdue Joint Research Center, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, China aff001;  Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, United States of America aff002
Vyšlo v časopise: Opposing functions of Fng1 and the Rpd3 HDAC complex in H4 acetylation in Fusarium graminearum. PLoS Genet 16(11): e32767. doi:10.1371/journal.pgen.1009185
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009185

Souhrn

Histone acetylation, balanced by histone acetyltransferase (HAT) and histone deacetylase (HDAC) complexes, affects dynamic transitions of chromatin structure to regulate transcriptional accessibility. However, little is known about the interplay between HAT and HDAC complexes in Fusarium graminearum, a causal agent of Fusarium Head Blight (FHB) that uniquely contains chromosomal regions enriched for house-keeping or infection-related genes. In this study, we identified the ortholog of the human inhibitor of growth (ING1) gene in F. graminearum (FNG1) and found that it specifically interacts with the FgEsa1 HAT of the NuA4 complex. Deletion of FNG1 led to severe growth defects and blocked conidiation, sexual reproduction, DON production, and plant infection. The fng1 mutant was normal in H3 acetylation but significantly reduced in H4 acetylation. A total of 34 spontaneous suppressors of fng1 with faster growth rate were isolated. Most of them were still defective in sexual reproduction and plant infection. Thirty two of them had mutations in orthologs of yeast RPD3, SIN3, and SDS3, three key components of the yeast Rpd3L HDAC complex. Four mutations in these three genes were verified to suppress the defects of fng1 mutant in growth and H4 acetylation. The rest two suppressor strains had a frameshift or nonsense mutation in a glutamine-rich hypothetical protein that may be a novel component of the FgRpd3 HDAC complex in filamentous fungi. FgRpd3, like Fng1, localized in euchromatin. Deletion of FgRPD3 resulted in severe growth defects and elevated H4 acetylation. In contract, the Fgsds3 deletion mutant had only a minor reduction in growth rate but FgSIN3 appeared to be an essential gene. RNA-seq analysis revealed that 48.1% and 54.2% of the genes with altered expression levels in the fng1 mutant were recovered to normal expression levels in two suppressor strains with mutations in FgRPD3 and FgSDS3, respectively. Taken together, our data showed that Fng1 is important for H4 acetylation as a component of the NuA4 complex and functionally related to the FgRpd3 HDAC complex for transcriptional regulation of genes important for growth, conidiation, sexual reproduction, and plant infection in F. graminearum.

Klíčová slova:

Acetylation – Fusarium graminearum – Gene expression – Histones – Nonsense mutation – Saccharomyces cerevisiae – Suppressor genes – Wheat


Zdroje

1. Eberharter A, Becker PB. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep. 2002;3(3):224–9. doi: 10.1093/embo-reports/kvf053 11882541.

2. Freitag M. Histone methylation by SET domain proteins in fungi. Annu Rev Microbiol. 2017;71:413–39. doi: 10.1146/annurev-micro-102215-095757 28715960

3. Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem. 2007;76:75–100. doi: 10.1146/annurev.biochem.76.052705.162114 17362198

4. Kurdistani SK, Grunstein M. Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol. 2003;4(4):276–84. doi: 10.1038/nrm1075 12671650

5. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, et al. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 1999;18(18):5108–19. doi: 10.1093/emboj/18.18.5108 10487762

6. Vicente-Muñoz S, Romero P, Magraner-Pardo L, Martinez-Jimenez CP, Tordera V, Pamblanco M. Comprehensive analysis of interacting proteins and genome-wide location studies of the Sas3-dependent NuA3 histone acetyltransferase complex. FEBS Open Bio. 2014;4:996–1006. doi: 10.1016/j.fob.2014.11.001 25473596

7. Doyon Y, Selleck W, Lane WS, Tan S, Côté J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol. 2004;24(5):1884–96. doi: 10.1128/mcb.24.5.1884-1896.2004 14966270

8. Howe L, Auston D, Grant P, John S, Cook RG, Workman JL, et al. Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 2001;15(23):3144–54. doi: 10.1101/gad.931401 11731478

9. Dubey A, Lee J, Kwon S, Lee Y-H, Jeon J. A MYST family histone acetyltransferase, MoSAS3, is required for development and pathogenicity in the rice blast fungus. Mol Plant Pathol. 2019;20(11):1491–505. doi: 10.1111/mpp.12856 31364260

10. Clarke AS, Lowell JE, Jacobson SJ, Pillus L. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol. 1999;19(4):2515–26. doi: 10.1128/mcb.19.4.2515 10082517

11. Soukup AA, Chiang YM, Bok JW, Reyes-Dominguez Y, Oakley BR, Wang CC, et al. Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol Microbiol. 2012;86(2):314–30. doi: 10.1111/j.1365-2958.2012.08195.x 22882998

12. Choy JS, Tobe BT, Huh JH, Kron SJ. Yng2p-dependent NuA4 histone H4 acetylation activity is required for mitotic and meiotic progression. J Biol Chem. 2001;276(47):43653–62. doi: 10.1074/jbc.M102531200 11544250

13. Howe L, Kusch T, Muster N, Chaterji R, Yates JR, Workman JL. Yng1p modulates the activity of Sas3p as a component of the yeast NuA3 histone acetyltransferase complex. Mol Cell Biol. 2002;22(14):5047–53. doi: 10.1128/mcb.22.14.5047-5053.2002 12077334

14. Loewith R, Meijer M, Lees-Miller SP, Riabowol K, Young D. Three yeast proteins related to the human candidate tumor suppressor p33(ING1) are associated with histone acetyltransferase activities. Mol Cell Biol. 2000;20(11):3807–16. doi: 10.1128/mcb.20.11.3807-3816.2000 10805724

15. Martin DGE, Baetz K, Shi X, Walter KL, MacDonald VE, Wlodarski MJ, et al. The Yng1p plant homeodomain finger is a methyl-histone binding module that recognizes lysine 4-methylated histone H3. Mol Cell Biol. 2006;26(21):7871–9. doi: 10.1128/MCB.00573-06 16923967

16. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, 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):785–96. doi: 10.1016/j.molcel.2006.10.026 17157260

17. Choy JS, Kron SJ. NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol Cell Biol. 2002;22(23):8215–25. doi: 10.1128/mcb.22.23.8215-8225.2002 12417725

18. Nourani A, Howe L, Pray-Grant MG, Workman JL, Grant PA, Côté J. Opposite role of yeast ING family members in p53-dependent transcriptional activation. J Biol Chem. 2003;278(21):19171–5. doi: 10.1074/jbc.C300036200 12672825

19. Kong X, van Diepeningen AD, van der Lee TAJ, Waalwijk C, Xu J, Xu J, et al. The Fusarium graminearum histone acetyltransferases are important for morphogenesis, DON biosynthesis, and pathogenicity. Front Microbiol. 2018;9:654. doi: 10.3389/fmicb.2018.00654 29755419

20. Lee Y, Min K, Son H, Park AR, Kim J-C, Choi GJ, et al. ELP3 is involved in sexual and asexual development, virulence, and the oxidative stress response in Fusarium graminearum. Mol Plant Microbe Interact. 2014;27(12):1344–55. doi: 10.1094/MPMI-05-14-0145-R 25083910

21. Chen Y, Wang J, Yang N, Wen Z, Sun X, Chai Y, et al. Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nat Commun. 2018;9(1):3429. doi: 10.1038/s41467-018-05683-7 30143616

22. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47(D1):D427–d32. Epub 2018/10/26. doi: 10.1093/nar/gky995 30357350

23. 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;317(5843):1400–2. doi: 10.1126/science.1143708 17823352

24. Villafana RT, Ramdass AC, Rampersad SN. Selection of Fusarium trichothecene toxin genes for molecular detection depends on TRI gene cluster organization and gene function. Toxins. 2019;11(1):36. doi: 10.3390/toxins11010036 30646506

25. Jiang C, Cao S, Wang Z, Xu H, Liang J, Liu H, et al. An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection. Nat Microbiol. 2019;4(9):1582–91. doi: 10.1038/s41564-019-0468-8 31160822

26. Tollervey D, Lehtonen H, Carmo-Fonseca M, Hurt EC. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 1991;10(3):573–83. doi: 10.1002/j.1460-2075.1991.tb07984.x 1825809

27. Klocko AD, Rountree MR, Grisafi PL, Hays SM, Adhvaryu KK, Selker EU. Neurospora importin α is required for normal heterochromatic formation and DNA methylation. PLoS Genet. 2015;11(3):e1005083. doi: 10.1371/journal.pgen.1005083 25793375

28. Connolly LR, Smith KM, Freitag M. The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet. 2013;9(10):e1003916. doi: 10.1371/journal.pgen.1003916 24204317

29. Chen X-F, Kuryan B, Kitada T, Tran N, Li J-Y, Kurdistani S, et al. The Rpd3 core complex is a chromatin stabilization module. Curr Biol. 2012;22(1):56–63. doi: 10.1016/j.cub.2011.11.042 22177115

30. Biswas D, Takahata S, Stillman DJ. Different genetic functions for the Rpd3(L) and Rpd3(S) complexes suggest competition between NuA4 and Rpd3(S). Mol Cell Biol. 2008;28(14):4445–58. doi: 10.1128/MCB.00164-08 18490440

31. 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;26(4):499–509. doi: 10.1101/gr.199877.115 26934920

32. Hammond TM, Xiao H, Boone EC, Perdue TD, Pukkila PJ, Shiu PKT. SAD3, a putative helicase required for meiotic silencing by unpaired DNA, interacts with other components of the silencing machinery. G3-Genes Genom Genet. 2011;1(5):369–76. doi: 10.1534/g3.111.000570 22384347

33. Gong XYJ, Yu Q, Duan K, Tong Y, Zhang XY, Mei QY, et al. Histone acetyltransferase Gcn5 regulates gene expression by promoting the transcription of histone methyltransferase SET1. BBA-Gene Regul Mech. 2020;1863(9):194603. doi: 10.1016/j.bbagrm.2020.194603 32663628

34. Zheng H, Zheng W, Wu C, Yang J, Xi Y, Xie Q, et al. Rab GTPases are essential for membrane trafficking-dependent growth and pathogenicity in Fusarium graminearum. Environ Microbiol. 2015;17(11):4580–99. doi: 10.1111/1462-2920.12982 26177389

35. Lee S-H, Han Y-K, Yun S-H, Lee Y-W. Roles of the glyoxylate and methylcitrate cycles in sexual development and virulence in the cereal pathogen Gibberella zeae. Eukaryot Cell. 2009;8(8):1155–64. doi: 10.1128/EC.00335-08 19525419

36. Shin JY, Bui D-C, Lee Y, Nam H, Jung S, Fang M, et al. Functional characterization of cytochrome P450 monooxygenases in the cereal head blight fungus Fusarium graminearum. Environ Microbiol. 2017;19(5):2053–67. doi: 10.1111/1462-2920.13730 28296081

37. León Ortiz AM, Reid RJD, Dittmar JC, Rothstein R, Nicolas A. Srs2 overexpression reveals a helicase-independent role at replication forks that requires diverse cell functions. DNA Repair. 2011;10(5):506–17. doi: 10.1016/j.dnarep.2011.02.004 21459050

38. Bhattacharya S, Esquivel BD, White TC. Overexpression or deletion of ergosterol biosynthesis genes alters doubling time, response to stress agents, and drug susceptibility in Saccharomyces cerevisiae. MBio. 2018;9(4):e01291–18. doi: 10.1128/mBio.01291-18 30042199

39. Chen J-Q, Li Y, Pan X, Lei B-K, Chang C, Liu Z-X, et al. The fission yeast inhibitor of growth (ING) protein Png1p functions in response to DNA damage. J Biol Chem. 2010;285(21):15786–93. doi: 10.1074/jbc.M110.101832 20299455

40. Lu Y, Su C, Mao X, Raniga PP, Liu H, Chen J. Efg1-mediated recruitment of NuA4 to promoters is required for hypha-specific Swi/Snf binding and activation in Candida albicans. Mol Biol Cell. 2008;19(10):4260–72. doi: 10.1091/mbc.e08-02-0173 18685084

41. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature. 2002;419(6905):411–5. doi: 10.1038/nature01035 12353039

42. Gómez EB, Nugent RL, Laria S, Forsburg SL. Schizosaccharomyces pombe histone acetyltransferase Mst1 (KAT5) is an essential protein required for damage response and chromosome segregation. Genetics. 2008;179(2):757–71. doi: 10.1534/genetics.107.085779 18505873

43. 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(3):438–49. doi: 10.1128/EC.00275-12 23355007

44. Cuzick A, Urban M, Hammond-Kosack K. Fusarium graminearum gene deletion mutants map1 and tri5 reveal similarities and differences in the pathogenicity requirements to cause disease on Arabidopsis and wheat floral tissue. New Phytol. 2008;177(4):990–1000. doi: 10.1111/j.1469-8137.2007.02333.x 18179606

45. Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, et al. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 2011;7(10):e1002310. doi: 10.1371/journal.ppat.1002310 22028654

46. Gao X, Jin Q, Jiang C, Li Y, Li C, Liu H, et al. FgPrp4 kinase is important for spliceosome B-complex activation and splicing efficiency in Fusarium graminearum. PLoS Genet. 2016;12(4):e1005973. doi: 10.1371/journal.pgen.1005973 27058959

47. Gao X, Zhang J, Song C, Yuan K, Wang J, Jin Q, et al. Phosphorylation by Prp4 kinase releases the self-inhibition of FgPrp31 in Fusarium graminearum. Curr Genet. 2018;64(6):1261–74. doi: 10.1007/s00294-018-0838-4 29671102

48. 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

49. Sun M, Zhang Y, Wang Q, Wu C, Jiang C, Xu J-R. The tri-snRNP specific protein FgSnu66 is functionally related to FgPrp4 kinase in Fusarium graminearum. Mol Microbiol. 2018;109(4):494–508. doi: 10.1111/mmi.14005 29923654

50. Ding S, Mehrabi R, Koten C, Kang Z, Wei Y, Seong K, et al. Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot Cell. 2009;8(6):867–76. doi: 10.1128/EC.00048-09 19377037

51. Zhou J, Zhou BO, Lenzmeier BA, Zhou J-Q. Histone deacetylase Rpd3 antagonizes Sir2-dependent silent chromatin propagation. Nucleic Acids Res. 2009;37(11):3699–713. doi: 10.1093/nar/gkp233 19372273

52. Lottersberger F, Panza A, Lucchini G, Longhese MP. Functional and physical interactions between yeast 14-3-3 proteins, acetyltransferases, and deacetylases in response to DNA replication perturbations. Mol Cell Biol. 2007;27(9):3266–81. doi: 10.1128/MCB.01767-06 17339336

53. Hodges AJ, Plummer DA, Wyrick JJ. NuA4 acetyltransferase is required for efficient nucleotide excision repair in yeast. DNA Repair. 2019;73:91–8. doi: 10.1016/j.dnarep.2018.11.006 30473425

54. Torres-Machorro AL, Pillus L. Bypassing the requirement for an essential MYST acetyltransferase. Genetics. 2014;197(3):851–63. Epub 2014/05/17. doi: 10.1534/genetics.114.165894 24831819

55. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–D30. doi: 10.1093/nar/gkt1223 24288371

56. Michelitsch MD, Weissman JS. A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc Natl Acad Sci. 2000;97(22):11910–5. doi: 10.1073/pnas.97.22.11910 11050225

57. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu J-R. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact. 2002;15(11):1119–27. doi: 10.1094/MPMI.2002.15.11.1119 12423017

58. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, et al. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. Plos Pathog. 2011;7(12):e1002460. doi: 10.1371/journal.ppat.1002460 22216007

59. Gardiner DM, Kazan K, Manners JM. Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet Biol. 2009;46(8):604–13. doi: 10.1016/j.fgb.2009.04.004 19406250

60. Zhou X, Li G, Xu J-R. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol Biol. 2011;722:199–212. doi: 10.1007/978-1-61779-040-9_15 21590423

61. Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol Plant Microbe Interact. 2007;20(6):627–36. doi: 10.1094/MPMI-20-6-0627 17555271

62. Zhang X-W, Jia L-J, Zhang Y, Jiang G, Li X, Zhang D, et al. In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell. 2012;24(12):5159–76. doi: 10.1105/tpc.112.105957 23266949

63. Yin T, Zhang Q, Wang J, Liu H, Wang C, Xu J-R, et al. The cyclase-associated protein FgCap1 has both protein kinase A-dependent and -independent functions during deoxynivalenol production and plant infection in Fusarium graminearum. Mol Plant Pathol. 2018;19(3):552–63. doi: 10.1111/mpp.12540 28142217

64. Wang H, Chen DP, Li CL, Tian N, Zhang J, Xu JR, et al. Stage-specific functional relationships between Tub1 and Tub2 beta-tubulins in the wheat scab fungus Fusarium graminearum. Fungal Genet Biol. 2019;132:103251. doi: 10.1016/j.fgb.2019.103251 31319136

65. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 22388286

66. 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;16:544. doi: 10.1186/s12864-015-1756-1 26198851

67. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943

68. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. Deriving the consequences of genomic variants with the ensembl API and SNP effect predictor. Bioinformatics. 2010;26(16):2069–70. doi: 10.1093/bioinformatics/btq330 20562413

69. Chen SF, Zhou YQ, Chen YR, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):884–90. doi: 10.1093/bioinformatics/bty560 30423086

70. Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44(W1):W160–W5. doi: 10.1093/nar/gkw257 27079975

71. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14(2):178–92. doi: 10.1093/bib/bbs017 22517427

72. Jiang C, Zhang C, Wu C, Sun P, Hou R, Liu H, et al. TRI6 and TRI10 play different roles in the regulation of deoxynivalenol (DON) production by cAMP signalling in Fusarium graminearum. Environ Microbiol. 2016;18(11):3689–701. doi: 10.1111/1462-2920.13279 26940955

73. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609

74. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. doi: 10.1038/nmeth.3317 25751142

75. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. doi: 10.1093/bioinformatics/btt656 24227677

76. Dimont E, Shi J, Kirchner R, Hide W. EdgeRun: an R package for sensitive, functionally relevant differential expression discovery using an unconditional exact test. Bioinformatics. 2015;31(15):2589–90. doi: 10.1093/bioinformatics/btv209 25900919

77. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–6. doi: 10.1093/bioinformatics/bti610 16081474

78. Ghosh D. Wavelet-based Benjamini-Hochberg procedures for multiple testing under dependence. Math Biosci Eng. 2019;17(1):56–72. doi: 10.3934/mbe.2020003 31731339

79. 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


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