Toward Understanding the Role of Chromatin in Secondary Metabolite Gene Regulation in the Rice Pathogen Fusarium fujikuroi

Studt, Lena

doi:10.1007/978-3-031-16503-0_12

Lena Studt⁷

Part of the book series: The Mycota ((MYCOTA,volume 5))

1052 Accesses

Abstract

Fusarium fujikuroi (teleomorph Gibberella fujikuroi) is a notorious rice pathogen and the causative agent of the bakanae (foolish seedling) disease. The symptoms of this disease, i.e., thin, chlorotic, and hyper-elongated rice internodes and often sterile grains, are due to the ability of this fungus to produce and secrete the phytohormones gibberellins (GAs). In addition to the GAs, F. fujikuroi produces a plethora of other secondary metabolites (SMs), including pigments but also potent mycotoxins. SMs are not essential for growth but may pose a selective advantage under certain environmental conditions, and as such are regulated by a complex gene regulatory network. The genes involved in the biosynthesis of individual SMs are physically linked in the fungal genome, thereby facilitating a coordinated and timely response when needed. Several of these regulatory components have been studied in F. fujikuroi. These include signal transduction pathways as well as narrow-domain and wide-domain transcriptional regulators. Another regulatory layer that has emerged as a key player in fungal SM gene regulation is chromatin structure. This chapter summarizes the current knowledge on SM biosynthesis in F. fujikuroi and the regulatory mechanisms that control their expression with a focus on chromatin structure.

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References

Ai X, Parthun MR (2004) The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol Cell 14:195–205. https://doi.org/10.1016/S1097-2765(04)00184-4
Article CAS Google Scholar
Allfrey V, Faulkner R, Mirsky A (1964) Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci 315:786–794. https://doi.org/10.1073/pnas.51.5.786
Article Google Scholar
Allis CD, Berger SL, Cote J et al (2007) New nomenclature for chromatin-modifying enzymes. Cell 131:633–636. https://doi.org/10.1016/j.cell.2007.10.039
Article CAS Google Scholar
Almouzni G, Cedar H (2016) Maintenance of epigenetic information. Cold Spring Harb Perspect Biol 8:19372–19373. https://doi.org/10.1101/cshperspect.a019372
Article CAS Google Scholar
Aoki T, O’Donnell K, Geiser DM (2014) Systematics of key phytopathogenic Fusarium species: current status and future challenges. J Gen Plant Pathol 80:189–201. https://doi.org/10.1007/s10327-014-0509-3
Article CAS Google Scholar
Arndt B, Janevska S, Schmid R et al (2017) A fungal N-dimethylallyltryptophan metabolite from Fusarium fujikuroi. Chembiochem 18:899–904. https://doi.org/10.1002/cbic.201600691
Article CAS Google Scholar
Atanasoff-Kardjalieff AK, Studt L (2022) Secondary metabolite gene regulation in mycotoxigenic Fusarium species: a focus on chromatin. Toxins (Basel) 14:96. https://doi.org/10.3390/toxins14020096
Article CAS Google Scholar
Atanasoff-Kardjalieff AK, Lünne F, Kalinina S et al (2021) Biosynthesis of fusapyrone depends on the H3K9 methyltransferase, FmKmt1, in Fusarium mangiferae. Front Fungal Biol 2:26. https://doi.org/10.3389/ffunb.2021.671796
Article Google Scholar
Bachleitner S, Sørensen JL, Gacek-Matthews A et al (2019) Evidence of a demethylase-independent role for the H3K4-specific histone demethylases in Aspergillus nidulans and Fusarium graminearum secondary metabolism. Front Microbiol 10:1759. https://doi.org/10.3389/fmicb.2019.01759
Article Google Scholar
Bachleitner S, Sulyok M, Sørensen JL et al (2021) The H4K20 methyltransferase Kmt5 is involved in secondary metabolism and stress response in phytopathogenic Fusarium species. Fungal Genet Biol 155. https://doi.org/10.1016/j.fgb.2021.103602
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395. https://doi.org/10.1038/cr.2011.22
Article CAS Google Scholar
Bannister AJ, Zegerman P, Partridge JF et al (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124. https://doi.org/10.1038/35065138
Article CAS Google Scholar
Becker PB, Workman JL (2013) Nucleosome remodeling and epigenetics. Cold Spring Harb Perspect Biol 5. https://doi.org/10.1101/cshperspect.a017905
Becker JS, Nicetto D, Zaret KS (2016) H3K9me3-dependent heterochromatin: barrier to cell fate changes. Trends Genet 32:29–41. https://doi.org/10.1016/j.tig.2015.11.001
Article CAS Google Scholar
Bicocca VT, Ormsby T, Adhvaryu KK et al (2018) ASH1-catalyzed H3K36 methylation drives gene repression and marks H3K27me2/3-competent chromatin. elife 7:e41497. https://doi.org/10.7554/eLife.41497
Article Google Scholar
Black JC, Van Rechem C, Whetstine JR (2012) Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell 48:491–507. https://doi.org/10.1016/j.molcel.2012.11.006
Article CAS Google Scholar
Bolton SL, Brannen PM, Glenn AE (2016) A novel population of Fusarium fujikuroi isolated from southeastern U.S. winegrapes reveals the need to re-evaluate the species’ fumonisin production. Toxins (Basel) 8:254. https://doi.org/10.3390/toxins8090254
Article CAS Google Scholar
Bömke C, Tudzynski B (2009) Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70:1876–1893. https://doi.org/10.1016/J.PHYTOCHEM.2009.05.020
Article Google Scholar
Bonner C, Sproule A, Rowland O et al (2021) DNA methylation is responsive to the environment and regulates the expression of biosynthetic gene clusters, metabolite production, and virulence in Fusarium graminearum. Front Fungal Biol 1:5. https://doi.org/10.3389/ffunb.2020.614633
Article Google Scholar
Briggs SD, Bryk M, Strahl BD et al (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15:3286–3295. https://doi.org/10.1101/gad.940201
Article CAS Google Scholar
Bryk M, Briggs SD, Strahl BD et al (2002) Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 12:165–170. https://doi.org/10.1016/S0960-9822(01)00652-2
Article CAS Google Scholar
Carter LLA, Leslie JF, Webster RK (2008) Population structure of Fusarium fujikuroi from California rice and water grass. Phytopathology 98:992–998. https://doi.org/10.1094/PHYTO-98-9-0992
Article CAS Google Scholar
Ćeranić A, Svoboda T, Berthiller F et al (2021) Identification and functional characterization of the gene cluster responsible for fusaproliferin biosynthesis in Fusarium proliferatum. Toxins (Basel) 13:468. https://doi.org/10.3390/toxins13070468
Article CAS Google Scholar
Chen Z, Ponts N (2020) H2A.Z and chromatin remodelling complexes: a focus on fungi. Crit Rev Microbiol 46:321–337. https://doi.org/10.1080/1040841X.2020.1781784
Article CAS Google Scholar
Chen Z, Zehraoui E, Atanasoff-Kardjalieff AK et al (2020) Effect of H2A.Z deletion is rescued by compensatory mutations in Fusarium graminearum. PLoS Genet:16:e1009125. https://doi.org/10.1371/journal.pgen.1009125
Chiara M, Fanelli F, Mulè G et al (2015) Genome sequencing of multiple isolates highlights subtelomeric genomic diversity within Fusarium fujikuroi. Genome Biol Evol 7:3062–3069. https://doi.org/10.1093/gbe/evv198
Article CAS Google Scholar
Chujo T, Scott B (2014) Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte-plant symbiosis. Mol Microbiol 92:413–434. https://doi.org/10.1111/mmi.12567
Article CAS Google Scholar
Connolly LR, Smith KM, Freitag M (2013) The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet 9:e1003916. https://doi.org/10.1371/journal.pgen.1003916
Article CAS Google Scholar
Craig JM (2005) Heterochromatin – many flavours, common themes. BioEssays 27:17–28. https://doi.org/10.1002/bies.20145
Article CAS Google Scholar
Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6:227
Article Google Scholar
Fang J, Feng Q, Ketel CS et al (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr Biol 12:1086–1099. https://doi.org/10.1016/S0960-9822(02)00924-7
Article CAS Google Scholar
Fingerman IM, Wu CL, Wilson BD, Briggs SD (2005) Global loss of Set1-mediated H3 Lys4 trimethylation is associated with silencing defects in Saccharomyces cerevisiae. J Biol Chem 280:28761–28765. https://doi.org/10.1074/jbc.C500097200
Article CAS Google Scholar
Freitag M (2017) Histone methylation by SET domain proteins in fungi. Annu Rev Microbiol 71:413–439. https://doi.org/10.1146/annurev-micro-102215-095757
Article CAS Google Scholar
Freitag M, Selker EU (2005) Controlling DNA methylation: many roads to one modification. Curr Opin Genet Dev 15:191–199. https://doi.org/10.1016/j.gde.2005.02.003
Article CAS Google Scholar
Freitag M, Hickey PC, Khlafallah TK et al (2004) HP1 is essential for DNA methylation in Neurospora. Mol Cell 13:427–434. https://doi.org/10.1016/S1097-2765(04)00024-3
Article CAS Google Scholar
Gacek-Matthews A, Noble LM, Gruber C et al (2015) KdmA, a histone H3 demethylase with bipartite function, differentially regulates primary and secondary metabolism in Aspergillus nidulans. Mol Microbiol 96:839–860. https://doi.org/10.1111/mmi.12977
Article CAS Google Scholar
Gacek-Matthews A, Berger H, Sasaki T et al (2016) 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 12:e1006222. https://doi.org/10.1371/journal.pgen.1006222
Article CAS Google Scholar
Gu Q, Ji T, Sun X et al (2017) Histone H3 lysine 9 methyltransferase FvDim5 regulates fungal development, pathogenicity and osmotic stress responses in Fusarium verticillioides. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx184
Hedden P, Sponsel V (2015) A century of Gibberellin research. J Plant Growth Regul 34:740–760
Article CAS Google Scholar
Ho JWK, Jung YL, Liu T et al (2014) Comparative analysis of metazoan chromatin organization. Nature 512:449–452. https://doi.org/10.1038/nature13415
Article CAS Google Scholar
Hori S (1890) Injurious fungi attacking rice plants. Bot Mag 4:425–427
Google Scholar
Jamieson K, Rountree MR, Lewis ZA et al (2013) Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Natl Acad Sci U S A 110:6027–6032. https://doi.org/10.1073/pnas.1303750110
Article CAS Google Scholar
Jamieson K, Wiles ET, McNaught KJ et al (2016) Loss of HP1 causes depletion of H3K27me3 from facultative heterochromatin and gain of H3K27me2 at constitutive heterochromatin. Genome Res 26:97–107. https://doi.org/10.1101/gr.194555.115
Article CAS Google Scholar
Janevska S, Arndt B, Niehaus E-M, Burkhardt I, Rösler SM, Brock NL, Humpf H-U, Dickschat JS, Tudzynski B (2016) Gibepyrone biosynthesis in the rice pathogen Fusarium fujikuroi is facilitated by a small polyketide synthase gene cluster. J Biol Chem 291(53):27403–27420. https://doi.org/10.1074/jbc.M116.753053
Article CAS Google Scholar
Janevska S, Arndt B, Baumann L et al (2017) Establishment of the inducible Tet-On system for the activation of the silent trichosetin gene cluster in Fusarium fujikuroi. Toxins (Basel) 9:126. https://doi.org/10.3390/toxins9040126
Article CAS Google Scholar
Janevska S, Baumann L, Sieber CMK et al (2018a) Elucidation of the two H3K36me3 histone methyltransferases Set2 and Ash1 in Fusarium fujikuroi unravels their different chromosomal targets and a major impact of Ash1 on genome stability. Genetics 208:153–171. https://doi.org/10.1534/genetics.117.1119
Article CAS Google Scholar
Janevska S, Güldener U, Sulyok M et al (2018b) Set1 and Kdm5 are antagonists for H3K4 methylation and regulators of the major conidiation-specific transcription factor gene ABA1 in Fusarium fujikuroi. Environ Microbiol 20:3343–3362. https://doi.org/10.1111/1462-2920.14339
Article CAS Google Scholar
Jeon Y-A, Yu S-H, Lee YY et al (2013) Incidence, molecular characteristics and pathogenicity of Gibberella fujikuroi species complex associated with rice seeds from Asian countries. Mycobiology 41:225–233. https://doi.org/10.5941/MYCO.2013.41.4.225
Article CAS Google Scholar
Jones RS, Gelbart WM (1993) The Drosophila Polycomb-group gene Enhancer of zeste contains a region with sequence similarity to trithorax. Mol Cell Biol 13:6357–6366. https://doi.org/10.1128/mcb.13.10.6357
Article CAS Google Scholar
Kakule TB, Sardar D, Lin Z, Schmidt EW (2013) Two related pyrrolidinedione synthetase loci in Fusarium heterosporum ATCC 74349 produce divergent metabolites. ACS Chem Biol 8:1549–1557. https://doi.org/10.1021/cb400159f
Article CAS Google Scholar
Keller NP (2019) Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol 17:167–180. https://doi.org/10.1038/s41579-018-0121-1
Article CAS Google Scholar
Keller NP, Hohn TM (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21:17–29. https://doi.org/10.1006/fgbi.1997.0970
Article CAS Google Scholar
Kizer KO, Phatnani HP, Shibata Y et al (2005) A novel domain in Set2 mediates RNA Polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25:3305–3316. https://doi.org/10.1128/mcb.25.8.3305-3316.2005
Article CAS Google Scholar
Klose RJ, Gardner KE, Liang G et al (2007) Demethylation of histone H3K36 and H3K9 by Rph1: a Vestige of an H3K9 methylation system in Saccharomyces cerevisiae ? Mol Cell Biol 27:3951–3961. https://doi.org/10.1128/mcb.02180-06
Article CAS Google Scholar
Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 80:868–871. https://doi.org/10.1126/science.184.4139.868
Article Google Scholar
Kourmouli N, Jeppesen P, Mahadevhaiah S et al (2004) Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J Cell Sci 117:2491–2501. https://doi.org/10.1242/jcs.01238
Article CAS Google Scholar
Krogan NJ, Dover J, Khorrami S et al (2002) COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 277:10753–10755. https://doi.org/10.1074/jbc.C200023200
Article CAS Google Scholar
Lachner M, O’Carroll D, Rea S et al (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120. https://doi.org/10.1038/35065132
Article CAS Google Scholar
Leslie JF, Summerell BA (2006) The fusarium laboratory manual. Blackwell Publishing, Ames, Iowa
Book Google Scholar
Leslie JF, Zeller KA, Logrieco A et al (2004) Species diversity of and toxin production by Gibberella fujikuroi species complex strains isolated from native prairie grasses in Kansas. Appl Environ Microbiol 70:2254–2262. https://doi.org/10.1128/AEM.70.4.2254-2262.2004
Article CAS Google Scholar
Lewis ZA (2017) Polycomb group systems in fungi: new models for understanding polycomb repressive complex 2. Trends Genet 33:220–231. https://doi.org/10.1016/j.tig.2017.01.006
Article CAS Google Scholar
Li B, Howe LA, Anderson S et al (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J Biol Chem 278:8897–8903. https://doi.org/10.1074/jbc.M212134200
Article CAS Google Scholar
Li L, Wright SJ, Krystofova S et al (2007) Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452. https://doi.org/10.1146/annurev.micro.61.080706.093432
Article CAS Google Scholar
Linnemannstöns P, Prado M, Fernández-Martín R et al (2002a) A carotenoid biosynthesis gene cluster in Fusarium fujikuroi: the genes carB and carRA. Mol Gen Genomics 267:593–602. https://doi.org/10.1007/s00438-002-0690-5
Article CAS Google Scholar
Linnemannstöns P, Schulte J, del Mar PM et al (2002b) The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet Biol 37:134–148. https://doi.org/10.1016/S1087-1845(02)00501-7
Article CAS Google Scholar
Macheleidt J, Mattern DJ, Fischer J et al (2016) Regulation and role of fungal secondary metabolites. Annu Rev Genet 50:371–392. https://doi.org/10.1146/annurev-genet-120215-035203
Article CAS Google Scholar
Marmorstein R, Zhou M-M (2014) Writers and readers of histone acetylation: structure, mechanism, and inhibition. Cold Spring Harb Perspect Biol 6:a018762. https://doi.org/10.1101/cshperspect.a018762
Article Google Scholar
Michielse CB, Studt L, Janevska S et al (2015) The global regulator FfSge1 is required for expression of secondary metabolite gene clusters but not for pathogenicity in Fusarium fujikuroi. Environ Microbiol 17:2690–2708. https://doi.org/10.1111/1462-2920.12592
Article CAS Google Scholar
Mihlan M, Homann V, Liu TWD, Tudzynski B (2003) AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Mol Microbiol 47:975–991. https://doi.org/10.1046/j.1365-2958.2003.03326.x
Article CAS Google Scholar
Möller M, Schotanus K, Soyer JL et al (2019) Destabilization of chromosome structure by histone H3 lysine 27 methylation. PLoS Genet 15:e1008093. https://doi.org/10.1371/journal.pgen.1008093
Article CAS Google Scholar
Morris SA, Shibata Y, Noma KI et al (2005) Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot Cell 4:1446–1454. https://doi.org/10.1128/EC.4.8.1446-1454.2005
Article CAS Google Scholar
Mosunova O, Navarro-Muñoz JC, Collemare J (2021) The biosynthesis of fungal secondary metabolites: from fundamentals to biotechnological applications. Encycl Mycol 458–476. https://doi.org/10.1016/B978-0-12-809633-8.21072-8
Musselman CA, Khorasanizadeh S, Kutateladze TG (2014) Towards understanding methyllysine readout. Biochim Biophys Acta – Gene Regul Mech 1839:686–693. https://doi.org/10.1016/j.bbagrm.2014.04.001
Article CAS Google Scholar
Nakayama J, Rice JC, Strahl BD, et al (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science (80) 292:110–113. https://doi.org/10.1126/science.1060118
Niehaus E-M, Kleigrewe K, Wiemann P et al (2013) Genetic manipulation of the Fusarium fujikuroi fusarin gene cluster yields insight into the complex regulation and fusarin biosynthetic pathway. Chem Biol 20:1055–1066. https://doi.org/10.1016/j.chembiol.2013.07.004
Article CAS Google Scholar
Niehaus E-M, Janevska S, von Bargen KW et al (2014a) Apicidin F: characterization and genetic manipulation of a new secondary metabolite gene cluster in the rice pathogen Fusarium fujikuroi. PLoS One 9:e103336. https://doi.org/10.1371/journal.pone.0103336
Article CAS Google Scholar
Niehaus EM, von Bargen KW, Espino JJ et al (2014b) Characterization of the fusaric acid gene cluster in Fusarium fujikuroi. Appl Microbiol Biotechnol 98:1749–1762. https://doi.org/10.1007/s00253-013-5453-1
Article CAS Google Scholar
Niehaus E-M, Münsterkötter M, Proctor RH et al (2016a) Comparative “Omics” of the Fusarium fujikuroi species complex highlights differences in genetic potential and metabolite synthesis. Genome Biol Evol 8:3574–3599. https://doi.org/10.1093/gbe/evw259
Article CAS Google Scholar
Niehaus E-M, Studt L, von Bargen KW et al (2016b) Sound of silence: the beauvericin cluster in Fusarium fujikuroi is controlled by cluster-specific and global regulators mediated by H3K27 modification. Environ Microbiol 18:4282–4302. https://doi.org/10.1111/1462-2920.13576
Article CAS Google Scholar
Niehaus E-M, Kim H-K, Münsterkötter M et al (2017a) Comparative genomics of geographically distant Fusarium fujikuroi isolates revealed two distinct pathotypes correlating with secondary metabolite profiles. PLoS Pathog 13:e1006670. https://doi.org/10.1371/journal.ppat.1006670
Article CAS Google Scholar
Niehaus EM, Schumacher J, Burkhardt I et al (2017b) The GATA-type transcription factor Csm1 regulates conidiation and secondary metabolism in Fusarium fujikuroi. Front Microbiol 8:1175. https://doi.org/10.3389/fmicb.2017.01175
Article Google Scholar
Niehaus E-M, Rindermann L, Janevska S et al (2018) Analysis of the global regulator Lae 1 uncovers a connection between Lae1 and the histone acetyltransferase HAT1 in Fusarium fujikuroi. Appl Microbiol Biotechnol 102:279–295. https://doi.org/10.1007/s00253-017-8590-0
Article CAS Google Scholar
Nirenberg HI, O’Donnell K (1998) New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 90:434. https://doi.org/10.2307/3761403
Article Google Scholar
Nishioka K, Rice JC, Sarma K et al (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 9:1201–1213. https://doi.org/10.1016/S1097-2765(02)00548-8
Article CAS Google Scholar
O’Donnell K, Ward TJ, Robert VARG et al (2015) DNA sequence-based identification of Fusarium: current status and future directions. Phytoparasitica 43:583–595. https://doi.org/10.1007/s12600-015-0484-z
Article Google Scholar
O’Donnell K, McCormick SP, Busman M et al (2018) Marasas et al. 1984 “Toxigenic Fusarium species: identity and mycotoxicology” revisited. Mycologia 110:1058–1080. https://doi.org/10.1080/00275514.2018.1519773
Article CAS Google Scholar
Palmer JM, Perrin RM, Dagenais TRT, Keller NP (2008) H3K9 methylation regulates growth and development in Aspergillus fumigatus. Eukaryot Cell 7:2052–2060. https://doi.org/10.1128/EC.00224-08
Article CAS Google Scholar
Park S-Y, Kim J-S (2020) A short guide to histone deacetylases including recent progress on class II enzymes. Exp Mol Med 52:204–212. https://doi.org/10.1038/s12276-020-0382-4
Article CAS Google Scholar
Pedrozo R, Fenoglio JJ, Little CR (2015) First report of seedborne Fusarium fujikuroi and its potential to cause pre- and post-emergent damping-off on soybean (Glycine max) in the United States. Plant Dis 99:1865–1865. https://doi.org/10.1094/PDIS-03-15-0321-PDN
Article Google Scholar
Pfannmüller A, Leufken J, Studt L et al (2017) Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi. PLoS One 12:e0176194. https://doi.org/10.1371/journal.pone.0176194
Article CAS Google Scholar
Pham KTM, Inoue Y, Van VB et al (2015) MoSET1 (histone H3K4 methyltransferase in Magnaporthe oryzae) regulates global gene expression during infection-related morphogenesis. PLoS Genet 11:e1005385. https://doi.org/10.1371/journal.pgen.1005385
Article CAS Google Scholar
Poveda A, Pamblanco M, Tafrov S et al (2004) Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J Biol Chem 279:16033–16043. https://doi.org/10.1074/jbc.M314228200
Article CAS Google Scholar
Pusztahelyi T, Holb IJ, Pócsi I (2015) Secondary metabolites in fungus-plant interactions. Front Plant Sci 6:573. https://doi.org/10.3389/fpls.2015.00573
Article Google Scholar
Reyes-Dominguez Y, Bok JW, Berger H et al (2010) Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol Microbiol 76:1376–1386. https://doi.org/10.1111/j.1365-2958.2010.07051.x
Article CAS Google Scholar
Ridenour JB, Möller M, Freitag M (2020) Polycomb repression without bristles: facultative heterochromatin and genome stability in fungi. Genes (Basel) 11:638. https://doi.org/10.3390/genes11060638
Article CAS Google Scholar
Rösler SM, Kramer K, Finkemeier I et al (2016a) The SAGA complex in the rice pathogen Fusarium fujikuroi: structure and functional characterization. Mol Microbiol 102:951–974. https://doi.org/10.1111/mmi.13528
Article CAS Google Scholar
Rösler SM, Sieber CMK, Humpf H-U, Tudzynski B (2016b) Interplay between pathway-specific and global regulation of the fumonisin gene cluster in the rice pathogen Fusarium fujikuroi. Appl Microbiol Biotechnol 100:5869–5882. https://doi.org/10.1007/s00253-016-7426-7
Article CAS Google Scholar
Ruiz-García AB, Sendra R, Galiana M et al (1998) Hat1 and Hat2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J Biol Chem 273:12599–12605. https://doi.org/10.1074/jbc.273.20.12599
Article Google Scholar
Sanders SL, Portoso M, Mata J et al (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603–614. https://doi.org/10.1016/j.cell.2004.11.009
Article CAS Google Scholar
Schotanus K, Soyer JL, Connolly LR et al (2015) Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenetics Chromatin 8:41. https://doi.org/10.1186/s13072-015-0033-5
Article CAS Google Scholar
Schotta G, Lachner M, Sarma K et al (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262. https://doi.org/10.1101/gad.300704
Article CAS Google Scholar
Schumacher J, Studt L, Tudzynski P (2019) The putative H3K36 demethylase BcKDM1 affects virulence, stress responses and photomorphogenesis in Botrytis cinerea. Fungal Genet Biol 123:14–24. https://doi.org/10.1016/J.FGB.2018.11.003
Article CAS Google Scholar
Seto E, Yoshida M (2014) Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6:a018713. https://doi.org/10.1101/cshperspect.a018713
Article Google Scholar
Shi Y, Lan F, Matson C et al (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953. https://doi.org/10.1016/j.cell.2004.12.012
Article CAS Google Scholar
Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81:65–95. https://doi.org/10.1146/annurev-biochem-051710-134100
Article CAS Google Scholar
Smith KM, Kothe GO, Matsen CB et al (2008) The fungus Neurospora crassa displays telomeric silencing mediated by multiple sirtuins and by methylation of histone H3 lysine 9. Epigenetics Chromatin 1:5. https://doi.org/10.1186/1756-8935-1-5
Article CAS Google Scholar
Stassen MJ, Bailey D, Nelson S et al (1995) The Drosophila trithorax proteins contain a novel variant of the nuclear receptor type DNA binding domain and an ancient conserved motif found in other chromosomal proteins. Mech Dev 52:209–223. https://doi.org/10.1016/0925-4773(95)00402-M
Article CAS Google Scholar
Strahl BD, Grant PA, Briggs SD et al (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22:1298–1306. https://doi.org/10.1128/mcb.22.5.1298-1306.2002
Article CAS Google Scholar
Studt L, Wiemann P, Kleigrewe K et al (2012) Biosynthesis of fusarubins accounts for pigmentation of Fusarium fujikuroi perithecia. Appl Environ Microbiol 78:4468–4480. https://doi.org/10.1128/AEM.00823-12
Article CAS Google Scholar
Studt L, Humpf H-U, Tudzynski B (2013a) Signaling governed by G proteins and cAMP is crucial for growth, secondary metabolism and sexual development in Fusarium fujikuroi. PLoS One 8:e58185. https://doi.org/10.1371/journal.pone.0058185
Article CAS Google Scholar
Studt L, Schmidt FJ, Jahn L et al (2013b) Two histone deacetylases, FfHda1 and FfHda2, are important for Fusarium fujikuroi secondary metabolism and virulence. Appl Environ Microbiol 79:7719–7734. https://doi.org/10.1128/AEM.01557-13
Article CAS Google Scholar
Studt L, Janevska S, Niehaus E-M et al (2016a) Two separate key enzymes and two pathway-specific transcription factors are involved in fusaric acid biosynthesis in Fusarium fujikuroi. Environ Microbiol 18:936–956. https://doi.org/10.1111/1462-2920.13150
Article CAS Google Scholar
Studt L, Rösler SM, Burkhardt I et al (2016b) Knock-down of the methyltransferase Kmt6 relieves H3K27me3 and results in induction of cryptic and otherwise silent secondary metabolite gene clusters in Fusarium fujikuroi. Environ Microbiol 18:4037–4054. https://doi.org/10.1111/1462-2920.13427
Article CAS Google Scholar
Studt L, Janevska S, Arndt B et al (2017) 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 07:2144. https://doi.org/10.3389/fmicb.2016.02144
Article Google Scholar
Sun S, Snyder WC (1981) The bakanae disease of the rice plant. In: Nelson E, Toussoun TA, Cook RJ (eds) Fusarium: diseases, biology and taxonomy. The Pennsylvania State University Press, University Park, pp 104–113
Google Scholar
Takahashi YH, Shilatifard A (2010) Structural basis for H3K4 trimethylation by yeast Set1/COMPASS. Adv Enzym Regul 50:104–110. https://doi.org/10.1016/j.advenzreg.2009.12.005
Article Google Scholar
Takahashi Y-h, Westfield GH, Oleskie a N et al (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc Natl Acad Sci 108:20526–20531. https://doi.org/10.1073/pnas.1109360108
Article CAS Google Scholar
Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283. https://doi.org/10.1038/35104508
Article CAS Google Scholar
Tang G, Yuan J, Wang J et al (2021) Fusarium BP1 is a reader of H3K27 methylation. Nucleic Acids Res 49:10448–10464. https://doi.org/10.1093/nar/gkab844
Article CAS Google Scholar
Tobiasen C, Aahman J, Ravnholt KS et al (2006) Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 51:43–58. https://doi.org/10.1007/s00294-006-0103-0
Article CAS Google Scholar
Tschiersch B, Hofmann A, Krauss V et al (1994) The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13:3822–3831. https://doi.org/10.1002/j.1460-2075.1994.tb06693.x
Article CAS Google Scholar
Tu S, Bulloch EMM, Yang L et al (2007) Identification of histone demethylases in Saccharomyces cerevisiae. J Biol Chem 282:14262–14271. https://doi.org/10.1074/jbc.M609900200
Article CAS Google Scholar
Varga J, Kocsubé S, Tóth B, Mesterházy Á (2005) Nonribosomal peptide synthetase genes in the genome of Fusarium graminearum, causative agent of wheat head blight. Acta Biol Hung 56:375–388. https://doi.org/10.1556/ABiol.56.2005.3-4.19
Article CAS Google Scholar
von Bargen KW, Niehaus EM, Bergander K et al (2013) Structure elucidation and antimalarial activity of apicidin F: an apicidin-like compound produced by Fusarium fujikuroi. J Nat Prod 76:2136–2140. https://doi.org/10.1021/np4006053
Article CAS Google Scholar
von Bargen KW, Niehaus E-M, Krug I, et al (2015) Isolation and structure elucidation of fujikurins A–D: products of the PKS19 gene cluster in Fusarium fujikuroi. J Nat Prod 78:1809–1815. doi:https://doi.org/10.1021/np5008137
Weiner A, Chen HV, Liu CL et al (2012) Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10:17. https://doi.org/10.1371/journal.pbio.1001369
Article CAS Google Scholar
Westphal KR, Bachleitner S, Severinsen MM et al (2021) Cyclic, hydrophobic hexapeptide fusahexin is the product of a nonribosomal peptide synthetase in Fusarium graminearum. J Nat Prod 84:2070–2080. https://doi.org/10.1021/acs.jnatprod.0c00947
Article CAS Google Scholar
Wiemann P, Willmann A, Straeten M et al (2009) Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi: genes, their function and regulation. Mol Microbiol 72:931–946. https://doi.org/10.1111/j.1365-2958.2009.06695.x
Article CAS Google Scholar
Wiemann P, Brown DW, Kleigrewe K et al (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77:972–994. https://doi.org/10.1111/j.1365-2958.2010.07263.x
Article CAS Google Scholar
Wiemann P, Sieber CMK, von Bargen KW et al (2013) Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog 9:e1003475. https://doi.org/10.1371/journal.ppat.1003475
Article CAS Google Scholar
Wiles ET, McNaught KJ, Kaur G et al (2020) Evolutionarily ancient BAH-PHD protein mediates Polycomb silencing. Proc Natl Acad Sci U S A 117:11614. https://doi.org/10.1073/pnas.1918776117
Article CAS Google Scholar
Yabuta T, Hayashi T (1939) Biochemical studies on the bakanae fungus of rice. II. Isolation of “Gibberellin”, the active principle which makes the rice seedlings grow slenderly. J Agric Chem Soc Jpn 15:257–266
CAS Google Scholar
Zhang X, Liu X, Zhao Y et al (2016) Histone H3 lysine 9 methyltransferase DIM5 is required for the development and virulence of Botrytis cinerea. Front Microbiol 7:1289. https://doi.org/10.3389/fmicb.2016.01289
Article Google Scholar

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Acknowledgment

I wish to express my gratitude to Bettina Tudzynski for introducing me to the beauty of molecular microbiology and for her long-term scientific support.

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Department of Applied Genetics and Cell Biology, Institute of Microbial Genetics, University of Natural Resources and Life Sciences, Vienna, Tulln an der Donau, Austria
Lena Studt

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Lena Studt
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School of Natural Sciences, Massey University, Palmerston North, New Zealand
Barry Scott
School of Agriculture and Environment, Massey University, Palmerston North, New Zealand
Carl Mesarich

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Studt, L. (2023). Toward Understanding the Role of Chromatin in Secondary Metabolite Gene Regulation in the Rice Pathogen Fusarium fujikuroi. In: Scott, B., Mesarich, C. (eds) Plant Relationships. The Mycota, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-031-16503-0_12

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DOI: https://doi.org/10.1007/978-3-031-16503-0_12
Published: 08 December 2022
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