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

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

doi:10.1073/pnas.1721381115

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

Journal Article · Wed Apr 11 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1721381115· OSTI ID:1625013

^[1]; Pelkmans, Jordi F. ^[2]; Ohm, Robin A. ^[2]; Vos, Aurin M. ^[2]; Sonnenberg, Anton S. M. ^[3]; Baars, Johan J. P. ^[3]; Wösten, Han A. B. ^[2];

^[1]; Abeel, Thomas ^[4]

Delft Univ. of Technology (Netherlands). Delft Bioinformatics Lab
Univ. of Utrecht (Netherlands). Microbiology
Wageningen Univ. and Research (Netherlands)
Delft Univ. of Technology (Netherlands). Delft Bioinformatics Lab; Broad Inst. of MIT and Harvard, Cambridge, MA (United States)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625013

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 17; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (41)

Isolation of the B? and B? mating-type loci of Schizophyllum commune Specht, Charles A. Current Genetics, Vol. 28, Issue 4 https://doi.org/10.1007/BF00326436	journal	September 1995
BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1. Hoff, Katharina J.; Lange, Simone; Lomsadze, Alexandre Bioinformatics, Vol. 32, Issue 5 https://doi.org/10.1093/bioinformatics/btv661	journal	November 2015
Heritable Individual-Specific and Allele-Specific Chromatin Signatures in Humans McDaniell, R.; Lee, B. K.; Song, L. Science, Vol. 328, Issue 5975 https://doi.org/10.1126/science.1184655	journal	March 2010
Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower Edger, Patrick P.; Smith, Ronald; McKain, Michael R. The Plant Cell, Vol. 29, Issue 9 https://doi.org/10.1105/tpc.17.00010	journal	August 2017
Production of schizophyllan glucan by Schizophyllum commune ATCC 38548 from detoxificated hydrolysate of rice hull Shu, Chin-Hang; Hsu, Hui-Ju Journal of the Taiwan Institute of Chemical Engineers, Vol. 42, Issue 3 https://doi.org/10.1016/j.jtice.2010.08.009	journal	May 2011
Biased Allelic Expression in Human Primary Fibroblast Single Cells Borel, Christelle; Ferreira, Pedro G.; Santoni, Federico The American Journal of Human Genetics, Vol. 96, Issue 1 https://doi.org/10.1016/j.ajhg.2014.12.001	journal	January 2015
The Genome of the Basidiomycetous Yeast and Human Pathogen Cryptococcus neoformans Loftus, B. J. Science, Vol. 307, Issue 5713 https://doi.org/10.1126/science.1103773	journal	February 2005
Heritable Individual-Specific and Allele-Specific Chromatin Signatures in Humans K., Lee, B.; S., Furey, T.; J., Scott, L. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/j7hn-s822	text	January 2010
The transcriptional regulator c2h2 accelerates mushroom formation in Agaricus bisporus Pelkmans, Jordi F.; Vos, Aurin M.; Scholtmeijer, Karin Applied Microbiology and Biotechnology, Vol. 100, Issue 16 https://doi.org/10.1007/s00253-016-7574-9	journal	May 2016
Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis) Boonanuntanasarn, Surintorn; Jangprai, Araya; Na-Nakorn, Uthairat Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61738-0	journal	March 2020
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1364-3703.2011.00783.x	journal	April 2012
Efficient string matching: an aid to bibliographic search Aho, Alfred V.; Corasick, Margaret J. Communications of the ACM, Vol. 18, Issue 6 https://doi.org/10.1145/360825.360855	journal	June 1975
Basic Local Alignment Search Tool Altschul, S. Journal of Molecular Biology, Vol. 215, Issue 3 https://doi.org/10.1006/jmbi.1990.9999	journal	October 1990
A Computational Workflow to Identify Allele-specific Expression and Epigenetic Modification in Maize Wei, Xiaoxing; Wang, Xiangfeng Genomics, Proteomics & Bioinformatics, Vol. 11, Issue 4 https://doi.org/10.1016/j.gpb.2013.05.006	journal	August 2013
Uncovering the abilities of A garicus bisporus to degrade plant biomass throughout its life cycle: Plant biomass degradation by Agaricus bisporus Patyshakuliyeva, Aleksandrina; Post, Harm; Zhou, Miaomiao Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12967	journal	August 2015
Regulation of Heterochromatic Silencing and Histone H3 Lysine-9 Methylation by RNAi Volpe, T. A. Science, Vol. 297, Issue 5588 https://doi.org/10.1126/science.1074973	journal	August 2002
Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche Morin, E.; Kohler, A.; Baker, A. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 43 https://doi.org/10.1073/pnas.1206847109	journal	October 2012
Analysis of allelic differential expression in human white blood cells Pant, P. V. K. Genome Research, Vol. 16, Issue 3 https://doi.org/10.1101/gr.4559106	journal	March 2006
Allele-specific gene expression differences in humans Buckland, P. R. Human Molecular Genetics, Vol. 13, Issue suppl_2 https://doi.org/10.1093/hmg/ddh227	journal	October 2004
Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis Kämper, Jörg; Kahmann, Regine; Bölker, Michael Nature, Vol. 444, Issue 7115 https://doi.org/10.1038/nature05248	journal	November 2006
An efficient gene deletion procedure for the mushroom-forming basidiomycete Schizophyllum commune Ohm, Robin A.; de Jong, Jan F.; Berends, Elsa World Journal of Microbiology and Biotechnology, Vol. 26, Issue 10 https://doi.org/10.1007/s11274-010-0356-0	journal	February 2010
Genetic manipulation of Aspergillus nidulans: heterokaryons and diploids for dominance, complementation and haploidization analyses Todd, Richard B.; Davis, Meryl A.; Hynes, Michael J. Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.113	journal	April 2007
Analyses of allele-specific gene expression in highly divergent mouse crosses identifies pervasive allelic imbalance Crowley, James J.; Zhabotynsky, Vasyl; Sun, Wei Nature Genetics, Vol. 47, Issue 4 https://doi.org/10.1038/ng.3222	journal	March 2015
A detailed analysis of the recombination landscape of the button mushroom Agaricus bisporus var. bisporus Sonnenberg, Anton S. M.; Gao, Wei; Lavrijssen, Brian Fungal Genetics and Biology, Vol. 93 https://doi.org/10.1016/j.fgb.2016.06.001	journal	August 2016
Study on development of Agaricus bisporus by fluorescent microscopy and scanning electron microscopy. Saksena, K. N.; Marino, R.; Haller, M. N. Journal of Bacteriology, Vol. 126, Issue 1 https://doi.org/10.1128/JB.126.1.417-428.1976	journal	January 1976
Intra-isolate genome variation in arbuscular mycorrhizal fungi persists in the transcriptome: Intra-isolate genome variation in AMF Boon, E.; Zimmerman, E.; Lang, B. F. Journal of Evolutionary Biology, Vol. 23, Issue 7 https://doi.org/10.1111/j.1420-9101.2010.02019.x	journal	June 2010
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Nature Precedings https://doi.org/10.1038/npre.2010.4282.2	journal	April 2010
The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology https://doi.org/10.1111/j.1364-3703.2012.2011.00783.x	journal	March 2012
An ultrastructural and autoradiographic study of stipe elongation inAgaricus bisporus Craig, G. D.; Newsam, R. J.; Gull, K. Protoplasma, Vol. 98, Issue 1-2 https://doi.org/10.1007/BF01676660	journal	March 1979
Genetic processes in arbuscular mycorrhizal fungi Pawlowska, Teresa E. FEMS Microbiology Letters, Vol. 251, Issue 2 https://doi.org/10.1016/j.femsle.2005.08.007	journal	October 2005
EVOLUTIONARY SIGNIFICANCE OF IMBALANCED NUCLEAR RATIOS WITHIN HETEROKARYONS OF THE BASIDIOMYCETE FUNGUS HETEROBASIDION PARVIPORUM James, Timothy Y.; Stenlid, Jan; Olson, Åke Evolution, Vol. 62, Issue 9 https://doi.org/10.1111/j.1558-5646.2008.00462.x	journal	September 2008
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus Lin, Kui; Limpens, Erik; Zhang, Zhonghua PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004078	journal	January 2014
The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliaeinfection by downregulation plant defense responses Sun, Chao; Shao, Yongqi; Vahabi, Khabat BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870-014-0268-5	journal	October 2014
FastUniq: A Fast De Novo Duplicates Removal Tool for Paired Short Reads Xu, Haibin; Luo, Xiang; Qian, Jun PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0052249	journal	December 2012
The Top 10 fungal pathogens in molecular plant pathology: Corrigendum Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology, Vol. 13, Issue 7 https://doi.org/10.1111/j.1364-3703.2012.00822.x	journal	July 2012
Using native and syntenically mapped cDNA alignments to improve de novo gene finding Stanke, Mario; Diekhans, Mark; Baertsch, Robert Bioinformatics, Vol. 24, Issue 5 https://doi.org/10.1093/bioinformatics/btn013	journal	January 2008
Extensive and coordinated control of allele-specific expression by both transcription and translation in Candida albicans Muzzey, D.; Sherlock, G.; Weissman, J. S. Genome Research, Vol. 24, Issue 6 https://doi.org/10.1101/gr.166322.113	journal	April 2014
Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack Babikova, Zdenka; Gilbert, Lucy; Bruce, Toby J. A. Ecology Letters, Vol. 16, Issue 7 https://doi.org/10.1111/ele.12115	journal	May 2013
The Mutualistic Fungus Piriformospora indica Protects Barley Roots from a Loss of Antioxidant Capacity Caused by the Necrotrophic Pathogen Fusarium culmorum Harrach, Borbála D.; Baltruschat, Helmut; Barna, Balázs Molecular Plant-Microbe Interactions®, Vol. 26, Issue 5 https://doi.org/10.1094/mpmi-09-12-0216-r	journal	May 2013

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Enabling community-based metrology for wood-degrading fungi Perez, Rolando; Luccioni, Marina; Kamakaka, Rohinton Fungal Biology and Biotechnology, Vol. 7, Issue 1 https://doi.org/10.1186/s40694-020-00092-2	journal	March 2020
Comparative Proteomic Analysis of Pleurotus ostreatus Reveals Great Metabolic Differences in the Cap and Stipe Development and the Potential Role of Ca2+ in the Primordium Differentiation Zhu, Weiwei; Hu, Jinbo; Li, Yang International Journal of Molecular Sciences, Vol. 20, Issue 24 https://doi.org/10.3390/ijms20246317	journal	December 2019
Investigating unexplained genetic variation and its expression in the arbuscular mycorrhizal fungus Rhizophagus irregularis: A comparison of whole genome and RAD sequencing data Masclaux, Frédéric G.; Wyss, Tania; Pagni, Marco PLOS ONE, Vol. 14, Issue 12 https://doi.org/10.1371/journal.pone.0226497	journal	December 2019
Aspergillus fumigatus and Aspergillosis in 2019 Latgé, Jean-Paul; Chamilos, Georgios Clinical Microbiology Reviews, Vol. 33, Issue 1 https://doi.org/10.1128/cmr.00140-18	journal	November 2019
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59 BASIC BIOLOGICAL SCIENCES
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RNA-seq
quantification

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

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