Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism
Fungi produce a plethora of secondary metabolites (SMs) involved in cellular protection, defense, and signaling. Like other metabolic processes, transcription of SM biosynthesis genes is tightly regulated to prevent an unnecessary use of resources. Genes involved in SM biosynthesis are usually physi...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01759/full |
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| author | Simone Bachleitner Jens Laurids Sørensen Agnieszka Gacek-Matthews Michael Sulyok Lena Studt Joseph Strauss |
| author_facet | Simone Bachleitner Jens Laurids Sørensen Agnieszka Gacek-Matthews Michael Sulyok Lena Studt Joseph Strauss |
| author_sort | Simone Bachleitner |
| collection | DOAJ |
| description | Fungi produce a plethora of secondary metabolites (SMs) involved in cellular protection, defense, and signaling. Like other metabolic processes, transcription of SM biosynthesis genes is tightly regulated to prevent an unnecessary use of resources. Genes involved in SM biosynthesis are usually physically linked, arranged in secondary metabolite gene clusters (SMGCs). Research over the last decades has shown that chromatin structure and posttranslational modifications (PTMs) of histones represent important layers of SMGC regulation. For instance, trimethylation of histone H3 lysine 4 (H3K4me3) is a PTM typically associated with promoter regions of actively transcribed genes. Previously, we have shown that the H3K4me3-specific, JmjC domain-containing histone demethylase KdmB functions not only in repression but also in activation of secondary metabolism in Aspergillus nidulans, suggesting that KdmB has additional functions apart from histone demethylation. In this study, we identified demethylase-independent functions of KdmB in transcriptional regulation of SM gene clusters. Furthermore, we show that this activating and demethylase-independent role of the H3K4 demethylase is also conserved in the phytopathogenic fungus Fusarium graminearum. Lack of FgKdm5 resulted in significant downregulation of five of seven analyzed SMs, whereby only one SMGC depends on a functional JmjC-domain. In A. nidulans strains deficient in H3K4 methylation, i.e., cclA∆, largely phenocopied kdmB∆, while this is not the case for most of the SMs analyzed in Fusarium spp. Notably, KdmB could not rescue the demethylase function in ∆fgkdm5 but restored all demethylase-independent phenotypes. |
| first_indexed | 2024-12-20T11:14:52Z |
| format | Article |
| id | doaj.art-67185471771741b59ff294bb649bef43 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-20T11:14:52Z |
| publishDate | 2019-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-67185471771741b59ff294bb649bef432022-12-21T19:42:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01759470903Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary MetabolismSimone Bachleitner0Jens Laurids Sørensen1Agnieszka Gacek-Matthews2Michael Sulyok3Lena Studt4Joseph Strauss5Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, AustriaDepartment of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, Aalborg, DenmarkDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, AustriaDepartment for Agrobiotechnology (IFA-Tulln), Institute of Bioanalytics and Agro-Metabolomics, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, AustriaDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, AustriaDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Vienna, AustriaFungi produce a plethora of secondary metabolites (SMs) involved in cellular protection, defense, and signaling. Like other metabolic processes, transcription of SM biosynthesis genes is tightly regulated to prevent an unnecessary use of resources. Genes involved in SM biosynthesis are usually physically linked, arranged in secondary metabolite gene clusters (SMGCs). Research over the last decades has shown that chromatin structure and posttranslational modifications (PTMs) of histones represent important layers of SMGC regulation. For instance, trimethylation of histone H3 lysine 4 (H3K4me3) is a PTM typically associated with promoter regions of actively transcribed genes. Previously, we have shown that the H3K4me3-specific, JmjC domain-containing histone demethylase KdmB functions not only in repression but also in activation of secondary metabolism in Aspergillus nidulans, suggesting that KdmB has additional functions apart from histone demethylation. In this study, we identified demethylase-independent functions of KdmB in transcriptional regulation of SM gene clusters. Furthermore, we show that this activating and demethylase-independent role of the H3K4 demethylase is also conserved in the phytopathogenic fungus Fusarium graminearum. Lack of FgKdm5 resulted in significant downregulation of five of seven analyzed SMs, whereby only one SMGC depends on a functional JmjC-domain. In A. nidulans strains deficient in H3K4 methylation, i.e., cclA∆, largely phenocopied kdmB∆, while this is not the case for most of the SMs analyzed in Fusarium spp. Notably, KdmB could not rescue the demethylase function in ∆fgkdm5 but restored all demethylase-independent phenotypes.https://www.frontiersin.org/article/10.3389/fmicb.2019.01759/fullKDM5histone demethylasesecondary metabolismAspergillus nidulansFusarium graminearumH3K4 methylation |
| spellingShingle | Simone Bachleitner Jens Laurids Sørensen Agnieszka Gacek-Matthews Michael Sulyok Lena Studt Joseph Strauss Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism Frontiers in Microbiology KDM5 histone demethylase secondary metabolism Aspergillus nidulans Fusarium graminearum H3K4 methylation |
| title | Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism |
| title_full | Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism |
| title_fullStr | Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism |
| title_full_unstemmed | Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism |
| title_short | Evidence of a Demethylase-Independent Role for the H3K4-Specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum Secondary Metabolism |
| title_sort | evidence of a demethylase independent role for the h3k4 specific histone demethylases in aspergillus nidulans and fusarium graminearum secondary metabolism |
| topic | KDM5 histone demethylase secondary metabolism Aspergillus nidulans Fusarium graminearum H3K4 methylation |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01759/full |
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