Nucleus-specific expression in the multinuclear mushroom-forming fungus Agaricus bisporus reveals different nuclear regulatory programs

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

doi:10.1073/pnas.1721381115

New Research In

Edited by Mitsuhiro Yanagida, Okinawa Institute of Science and Technology Graduate University, Onna-Son, Kunigami, Japan, and approved March 22, 2018 (received for review December 13, 2017)

Significance

Fungi are a broad class of organisms that play crucial roles in a wide variety of natural and industrial processes. Some are also harmful, destroying crops or infecting immunocompromised patients. Many fungi, at some point during their life cycle, contain two different nuclei, each with different genetic content. We examine the regulation of genes from these nuclei in a mushroom-forming fungus. We find that these nuclei contribute differently to the regulation of the fungal cells, and may therefore have a different impact on their environment. Furthermore, these differences change throughout the development of different tissues. This work contributes to our understanding of fungal physiology by examining this process.

Abstract

Many fungi are polykaryotic, containing multiple nuclei per cell. In the case of heterokaryons, there are different nuclear types within a single cell. It is unknown what the different nuclear types contribute in terms of mRNA expression levels in fungal heterokaryons. Each cell of the mushroom Agaricus bisporus contains two to 25 nuclei of two nuclear types originating from two parental strains. Using RNA-sequencing data, we assess the differential mRNA contribution of individual nuclear types and its functional impact. We studied differential expression between genes of the two nuclear types, P1 and P2, throughout mushroom development in various tissue types. P1 and P2 produced specific mRNA profiles that changed through mushroom development. Differential regulation occurred at the gene level, rather than at the locus, chromosomal, or nuclear level. P1 dominated mRNA production throughout development, and P2 showed more differentially up-regulated genes in important functional groups. In the vegetative mycelium, P2 up-regulated almost threefold more metabolism genes and carbohydrate active enzymes (cazymes) than P1, suggesting phenotypic differences in growth. We identified widespread transcriptomic variation between the nuclear types of A. bisporus. Our method enables studying nucleus-specific expression, which likely influences the phenotype of a fungus in a polykaryotic stage. Our findings have a wider impact to better understand gene regulation in fungi in a heterokaryotic state. This work provides insight into the transcriptomic variation introduced by genomic nuclear separation.

Footnotes

↵¹To whom correspondence may be addressed. Email: t.abeel{at}tudelft.nl or t.gehrmann{at}tudelft.nl.
↵²Present address: Department of Biotechnology, Delft University of Technology, 2629 HZ Delft, The Netherlands.

Author contributions: T.G., H.A.B.W., M.J.T.R., and T.A. designed research; T.G., J.F.P., R.A.O., A.M.V., A.S.M.S., J.J.P.B., H.A.B.W., M.J.T.R., and T.A. performed research; T.G. and R.A.O. analyzed data; and T.G., H.A.B.W., M.J.T.R., and T.A. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Methylation data have been deposited in the Sequence Read Archive (accession no. SAMN06284058).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1721381115/-/DCSupplemental.

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