Functional genomics of morphogenesis in filamentous ascomycetes
Evolution and Systematics of Plants and Fungi
Plant Genetics and Genomics
Final Report Abstract
The aim of the project was to identify molecular factors and mechanisms that regulate fruiting body development in filamentous ascomycetes. Fruiting bodies are complex multicellular structures that function in the production and dispersal of sexual spores, and they contain a number of cell types that are not found in vegetative mycelium. One avenue towards a deeper understanding of the molecular basis of fungal fruiting body development is the identification of genes that are differentially expressed during this process. In contrast to analyses involving only one species, comparative expression studies allow the identification of genes with evolutionary conserved expression patterns, which might be part of core modules of developmental regulation. The first phase of the project therefore aimed at using comparative transcriptomics to identify genes with evolutionary conserved expression patterns to identify core cellular processes underlying development as well as target genes for downstream functional analyses. Among the genes that were found to be upregulated during development across three species (Sordaria macrospora, Pyronema confluens and Ascodesmis nigricans) were a number of genes with predicted roles in chromatin organization or the regulation of gene expression, and these were the focus of the second phase of the project. In this phase, we performed more detailed molecular analyses of (putative) chromatin modifier and transcription factor genes in S. macrospora. Transcriptomics and cell and molecular biology analyses of these genes showed that asm2 (encodes a transcription factor) and asm3 (encodes a zf-MYND domain protein) have similarities in their expression patterns and their phenotypes during late developmental stages, whereas spt3 (encodes a subunit of the SAGA transcriptional co-activator) is involved in early steps of fruiting body development. We also performed in-depths analyses of asf1, a gene encoding a histone chaperone, and were able to show that actual histone binding of the ASF1 protein is required for fruiting body development, but not for genome stability, another process that ASF1 is involved in. We could also show that the histone acetyltransferase RTT109 plays a similar role as ASF1 in fruiting body development. Bioinformatics techniques that were developed in this project were applied in several collaborations for the analysis of fungal development and evolution as well as for the analysis of genome and transcriptome data of non-fungal organisms.
Publications
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Fungal genome and mating system transitions facilitated by chromosomal translocations involving intercentromeric recombination. PLOS Biology, 15(8), e2002527.
Sun, Sheng; Yadav, Vikas; Billmyre, R. Blake; Cuomo, Christina A.; Nowrousian, Minou; Wang, Liuyang; Souciet, Jean-Luc; Boekhout, Teun; Porcel, Betina; Wincker, Patrick; Granek, Joshua A.; Sanyal, Kaustuv & Heitman, Joseph
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Mating‐type factor‐specific regulation of the fumagillin/pseurotin secondary metabolite supercluster in Aspergillus fumigatus. Molecular Microbiology, 110(6), 1045-1065.
Yu, Yidong; Blachowicz, Adriana; Will, Cornelia; Szewczyk, Edyta; Glenn, Steven; Gensberger‐Reigl, Sabrina; Nowrousian, Minou; Wang, Clay C. C. & Krappmann, Sven
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Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nature Ecology & Evolution, 2(12), 1956-1965.
Murat, Claude; Payen, Thibaut; Noel, Benjamin; Kuo, Alan; Morin, Emmanuelle; Chen, Juan; Kohler, Annegret; Krizsán, Krisztina; Balestrini, Raffaella; Da Silva, Corinne; Montanini, Barbara; Hainaut, Mathieu; Levati, Elisabetta; Barry, Kerrie W.; Belfiori, Beatrice; Cichocki, Nicolas; Clum, Alicia; Dockter, Rhyan B.; Fauchery, Laure; ... & Martin, Francis M.
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The secreted metabolome of Streptomyces chartreusis and implications for bacterial chemistry. Proceedings of the National Academy of Sciences, 115(10), 2490-2495.
Senges, Christoph H. R.; Al-Dilaimi, Arwa; Marchbank, Douglas H.; Wibberg, Daniel; Winkler, Anika; Haltli, Brad; Nowrousian, Minou; Kalinowski, Jörn; Kerr, Russell G. & Bandow, Julia E.
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Combination of Proteogenomics with Peptide De Novo Sequencing Identifies New Genes and Hidden Posttranscriptional Modifications. mBio, 10(5).
Blank-Landeshammer, B.; Teichert, I.; Märker, R.; Nowrousian, M.; Kück, U. & Sickmann, A.
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Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes. Genetics, 213(4), 1545-1563.
Lütkenhaus, Ramona; Traeger, Stefanie; Breuer, Jan; Carreté, Laia; Kuo, Alan; Lipzen, Anna; Pangilinan, Jasmyn; Dilworth, David; Sandor, Laura; Pöggeler, Stefanie; Gabaldón, Toni; Barry, Kerrie; Grigoriev, Igor V. & Nowrousian, Minou
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Convergent evolution of linked mating-type loci in basidiomycete fungi. PLOS Genetics, 15(9), e1008365.
Sun, Sheng; Coelho, Marco A.; Heitman, Joseph & Nowrousian, Minou
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Genetic and Genomic Analyses Reveal Boundaries between Species Closely Related to Cryptococcus Pathogens. mBio, 10(3).
Passer, Andrew Ryan; Coelho, Marco A.; Billmyre, Robert Blake; Nowrousian, Minou; Mittelbach, Moritz; Yurkov, Andrey M.; Averette, Anna Floyd; Cuomo, Christina A.; Sun, Sheng & Heitman, Joseph
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Degradative Capacity of Two Strains of Rhodonia placenta: From Phenotype to Genotype. Frontiers in Microbiology, 11.
Kölle, Martina; Horta, Maria Augusta Crivelente; Nowrousian, Minou; Ohm, Robin A.; Benz, J. Philipp & Pilgård, Annica
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Endoplasmic reticulum membrane receptors of the GET pathway are conserved throughout eukaryotes. Proceedings of the National Academy of Sciences, 118(1).
Asseck, Lisa Yasmin; Mehlhorn, Dietmar Gerald; Monroy, Jhon Rivera; Ricardi, Martiniano Maria; Breuninger, Holger; Wallmeroth, Niklas; Berendzen, Kenneth Wayne; Nowrousian, Minou; Xing, Shuping; Schwappach, Blanche; Bayer, Martin & Grefen, Christopher
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Long transposon-rich centromeres in an oomycete reveal divergence of centromere features in Stramenopila-Alveolata-Rhizaria lineages. PLOS Genetics, 16(3), e1008646.
Fang, Yufeng; Coelho, Marco A.; Shu, Haidong; Schotanus, Klaas; Thimmappa, Bhagya C.; Yadav, Vikas; Chen, Han; Malc, Ewa P.; Wang, Jeremy; Mieczkowski, Piotr A.; Kronmiller, Brent; Tyler, Brett M.; Sanyal, Kaustuv; Dong, Suomeng; Nowrousian, Minou & Heitman, Joseph
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Draft genome sequences of strains CBS6241 and CBS6242 of the basidiomycetous yeastFilobasidium floriforme. G3 Genes|Genomes|Genetics, 12(2).
Guerreiro, Marco Alexandre; Ahrendt, Steven; Pangilinan, Jasmyn; Chen, Cindy; Yan, Mi; Lipzen, Anna; Barry, Kerrie; Grigoriev, Igor V.; Begerow, Dominik & Nowrousian, Minou
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Functional characterization of the developmental genes asm2, asm3, and spt3 required for fruiting body formation in the filamentous ascomycete Sordaria macrospora. Genetics, 219(2).
Lütkenhaus, Ramona; Breuer, Jan & Nowrousian, Minou
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Draft genome of the aardaker (Lathyrus tuberosus L.), a tuberous legume. BMC Genomic Data, 23(1).
Flood, Pádraic J.; Nowrousian, Minou; Huettel, Bruno; Woehle, Christian; Becker, Kerstin; Wollenweber, Tassilo Erik; Begerow, Dominik & Grefen, Christopher
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Obligate sexual reproduction of a homothallic fungus closely related to the Cryptococcus pathogenic species complex. eLife, 11.
Passer, Andrew Ryan; Clancey, Shelly Applen; Shea, Terrance; David-Palma, Márcia; Averette, Anna Floyd; Boekhout, Teun; Porcel, Betina M.; Nowrousian, Minou; Cuomo, Christina A.; Sun, Sheng; Heitman, Joseph & Coelho, Marco A.
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Functional analysis of chromatin-associated proteins in Sordaria macrospora reveals similar roles for RTT109 and ASF1 in development and DNA damage response. G3: Genes, Genomes, Genetics, 14(3).
Breuer, Jan; Ferreira, David Emanuel Antunes; Kramer, Mike; Bollermann, Jonas & Nowrousian, Minou
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Histone binding of ASF1 is required for fruiting body development but not for genome stability in the filamentous fungus Sordaria macrospora. mBio, 15(1).
Breuer, Jan; Busche, Tobias; Kalinowski, Jörn & Nowrousian, Minou
