The role of histone chaperones and specific transcription factors during multicellular development of filamentous ascomycetes
Final Report Abstract
Fungi (Eumycota) are are one of the most species-rich groups within the eukaryotes with a huge impact on nearly all ecosystems as well as for agriculture, medicine, pharmacology and biotechnology. Interestingly, most symbiotic or pathogenic interactions as well as the production of pharmaceutically or biotechnologically relevant metabolites are restricted to specific stages of the fungal life cycle. Therefore, the analysis of fungal differentiation processes is essential for understanding the impact of fungi on ecology including human life as well as for the use of fungi in biotechnological applications. As part of the project, we performed functional characterizations of the developmental genes ASF1 and PRO44, encoding a histone chaperone and a transcription factor, respectively. As both PRO44 and ASF1 are predicted to act on the regulation of gene expression in the nucleus, and mutants in both genes are blocked at the same stage of development, the starting hypothesis for this project was that PRO44 and ASF1 might be involved in similar aspects of transcriptional regulation. However, transcriptomics analyses revealed strikingly different patterns of gene expression in the two corresponding mutants, indicating distinct roles for the transcription factor PRO44 and the histone chaperone ASF1 in the regulation of sexual development in fungi. Furthermore, micrococcal nuclease sequencing showed that overall nucleosome positioning is not different in the wild type and the asf1 mutant, whereas bisulfite sequencing revealed a decrease in DNA methylation in ∆asf1, which might be a reason for the observed changes in gene expression. Transcriptome analysis of gene expression in young fruiting bodies showed that pro44 is required for correct expression of genes involved in extracellular metabolism. Deletion of the putative transcription factor gene asm2, which is downregulated in young fruiting bodies of ∆pro44, results in defects during ascospore maturation. As pro44 expression in young fruiting bodies is dependent on the presence of the transcription factor gene pro1, these data indicate that the transcription factors PRO1, PRO44, and ASM2 might be part of a gene regulatory network that governs fruiting body formation. Bioinformatics techniques that were developed in this project were applied to or adapted for a number of collaborative projects for the analysis of fungal development as well as one metagenomic project. In one collaborative project, we studied the recently discovered phenomenon of A-to-I RNA editing during sexual development in filamentous ascomycetes, and in a second project the sequencing of a sterile mutant genome led to the discovery of a new nuclear factor involved in fruiting body develoment in S. macrospora. An international collaboration with groups from the University of Singapore and the University of California resulted in insights into the evolution of multicellular development in fungi through comparative genomics of the Neolecta irregularis genome. Furthermore, in a collaboration with researchers from the Ruhr-University Bochum, a metagenome was assembled and used in combination with metaproteomics data were used to identify novel lipolytic enzymes from soil samples.
Publications
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(2018) The transcription factor PRO44 and the histone chaperone ASF1 regulate distinct aspects of multicellular development in the filamentous fungus Sordaria macrospora. BMC genetics 19 (1) 112
Schumacher, David Immanuel; Lütkenhaus, Ramona; Altegoer, Florian; Teichert, Ines; Kück, Ulrich; Nowrousian, Minou
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(2014) The filamentous fungus Sordaria macrospora as a genetic model to study fruiting body development. Adv Genet 87: 199-244
Teichert I, Nowrousian M, Pöggeler S, Kück U
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(2016) Complete mitochondrial genome sequence of the Pezizomycete Pyronema confluens. Genome Announc 4: e00355-16
Nowrousian M
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(2017) Innovation and constraint leading to complex multicellularity in the Ascomycota. Nat Commun 8:14444
Nguyen TA, Cissé OH, Wong JY, Zheng P, Hewitt D, Nowrousian M, Stajich JE, Jedd G
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(2017) New insights from an old mutant: SPADIX4 governs fruiting body development but not hyphal fusion in Sordaria macrospora. Mol Genet Genomics 292: 93-104
Teichert I, Lutomski M, Märker R, Nowrousian M, Kück U
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(2017) RNA editing during sexual development occurs in distantly related filamentous ascomycetes. Genome Biol Evol 9: 855-868
Teichert I, Dahlmann T, Kück U, Nowrousian M
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(2017) Simple discovery of bacterial biocatalysts from environmental samples through functional metaproteomics. Microbiome 5:28
Sukul P, Schäkermann S, Bandow JE, Kusnezowa A, Nowrousian M, Leichert LI
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(2018) Fruiting body development in ascomycetes. In: Anke T, Schüffler A (eds) The Mycota XV, Physiology and Genetics, 2nd edition, Springer-Verlag Berlin- Heidelberg, p. 1-56
Pöggeler S, Nowrousian M, Teichert I, Beier A, Kück U
