Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom forming fungi (Agaricomycetes)
- Biological Research Center, Hungary
- University of Pennsylvania, United States
- Ohio State University, United States
- Hungarian University of Agriculture and Life Sciences, Hungary
Abstract
Multicellularity has been one of the most important innovations in the history of life. The role of gene regulatory changes in driving transitions to multicellularity is being increasingly recognized; however, factors influencing gene expression patterns are poorly known in many clades. Here we compared the developmental transcriptomes of complex multicellular fruiting bodies of eight Agaricomycetes and Cryptococcus neoformans, a closely related human pathogen with a simple morphology. In-depth analysis in Pleurotus ostreatus revealed that allele-specific expression, natural antisense transcripts and developmental gene expression, but not RNA editing or a 'developmental hourglass' act in concert to shape its transcriptome during fruiting body development. We found that transcriptional patterns of genes strongly depend on their evolutionary ages. Young genes showed more developmental and allele-specific expression variation, possibly because of weaker evolutionary constraint, suggestive of non-adaptive expression variance in fruiting bodies. These results prompted us to define a set of conserved genes specifically regulated only during complex morphogenesis by excluding young genes and accounting for deeply conserved ones shared with species showing simple sexual development. Analysis of the resulting gene set revealed evolutionary and functional associations with complex multicellularity, which allowed us to speculate they are involved in complex multicellular morphogenesis of mushroom fruiting bodies.
Data availability
Raw RNA-Seq reads have been deposited to NCBI's GEO archive (GSE176181).
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Data from: Gene age predicts the transcriptional landscape of sexual morphogenesis in multicellular fungiDryad Digital Repository, doi:10.5061/dryad.5qfttdz5m.
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Gene age predicts the transcriptional landscape of sexual morphogenesis in multicellular fungiNCBI Gene Expression Omnibus, GSE176181.
Article and author information
Author details
Funding
Hungarian National Research, Development, and Innovation Office (GINOP-2.3.2-15-2016-00052)
- László G Nagy
Momentum program of the Hungarian Academy of Science (LP2019-13/2019)
- László G Nagy
European Research Council (758161)
- László G Nagy
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Luis F Larrondo, Pontificia Universidad Católica de Chile, Chile
Version history
- Preprint posted: June 6, 2021 (view preprint)
- Received: June 17, 2021
- Accepted: February 11, 2022
- Accepted Manuscript published: February 14, 2022 (version 1)
- Version of Record published: March 3, 2022 (version 2)
Copyright
© 2022, Merényi et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom forming fungi (Agaricomycetes)
eLife 11:e71348.
https://doi.org/10.7554/eLife.71348
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