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Nucleus Specific Expression In The Multinucleated Mushroom-Forming Fungus Agaricus bisporus Reveals Different Nuclear Regulatory Programs

By Thies Gehrmann, Jordi F Pelkmans, Robin A. Ohm, Aurin M. Vos, Anton S. M. Sonnenberg, Johan J. P. Baars, Han A B Wösten, Marcel J.T. Reinders, Thomas Abeel

Posted 29 May 2017
bioRxiv DOI: 10.1101/141689 (published DOI: 10.1073/pnas.1721381115)

Motivation: Fungi are essential in nutrient recycling in nature. They also form symbiotic, commensal, parasitic and pathogenic interactions with other organisms including plants, animals and humans. Many fungi are polykaryotic, containing multiple nuclei per cell. In the case of heterokaryons, there are even different nuclear types within a cell. It is unknown what the different nuclear types contribute in terms of mRNA expression levels in fungal heterokaryons. Each cell of the cultivated, mushroom forming basidiomycete Agaricus bisporus contains 2 to 25 nuclei of two nuclear types that originate from two parental strains. Using RNA-Seq data, we wish to assess the differential mRNA contribution of individual nuclear types in heterokaryotic cells and its functional impact. Results: We studied differential expression between genes of the two nuclear types throughout mushroom development of A. bisporus in various tissue types. The two nuclear types, P1 and P2, produced specific mRNA profiles which changed through development of the mushroom. The differential regulation occurred at the gene level, rather than at locus, chromosomal or nuclear level. Although the P1 nuclear type dominates the mRNA production throughout development, the P2 type showed more differentially upregulated genes in important functional groups including genes involved in metabolism and genes encoding secreted proteins. Out of 5,090 karyolelle pairs, i.e. genes with different alleles in the two nuclear types, 411 were differentially expressed, of which 246 were up-regulated by the P2 type. In the vegetative mycelium, the P2 nucleus up-regulated almost three-fold more metabolic genes and cazymes than P1, suggesting phenotypic differences in growth. A total of 10% of the differential karyollele expression is associated with differential methylation states, indicating that epigenetic mechanisms may be partly responsible for nuclear specific expression. Conclusion: We have identified widespread transcriptomic variation between the two nuclear types of A. bisporus. Our novel method enables studying karyollelle specific expression which likely influences the phenotype of a fungus in a polykaryotic stage. This is thus relevant for the performance of these fungi as a crop and for improving this species for breeding. Our findings could have a wider impact to better understand fungi as pathogens. This work provides the first insight into the transcriptomic variation introduced by genomic nuclear separation.

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