1. Developmental Biology
  2. Evolutionary Biology

Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom forming fungi (Agaricomycetes)

  1. Zsolt Merényi
  2. Máté Virágh
  3. Emile Gluck-Thaler
  4. Jason C Slot
  5. Brigitta Kiss
  6. Torda Varga
  7. András Geösel
  8. Botond Hegedüs
  9. Balázs Bálint
  10. László G Nagy  Is a corresponding author
  1. Biological Research Center, Hungary
  2. University of Pennsylvania, United States
  3. Ohio State University, United States
  4. Hungarian University of Agriculture and Life Sciences, Hungary
https://doi.org/10.7554/eLife.71348
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  1. Zsolt Merényi
  2. Máté Virágh
  3. Emile Gluck-Thaler
  4. Jason C Slot
  5. Brigitta Kiss
  6. Torda Varga
  7. András Geösel
  8. Botond Hegedüs
  9. Balázs Bálint
  10. László G Nagy
(2022)
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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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).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Zsolt Merényi

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  2. Máté Virágh

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  3. Emile Gluck-Thaler

    Department of Biology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Jason C Slot

    Department of Plant Pathology, Ohio State University, Columbus, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6731-3405

  5. Brigitta Kiss

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  6. Torda Varga

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  7. András Geösel

    Department of Vegetable and Mushroom Growing, Hungarian University of Agriculture and Life Sciences, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  8. Botond Hegedüs

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  9. Balázs Bálint

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.

  10. László G Nagy

    Synthetic and Systems Biology Unit, Biological Research Center, Szeged, Hungary
    For correspondence
    lnagy@fungenomelab.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4102-8566

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.

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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  1. Zsolt Merényi
  2. Máté Virágh
  3. Emile Gluck-Thaler
  4. Jason C Slot
  5. Brigitta Kiss
  6. Torda Varga
  7. András Geösel
  8. Botond Hegedüs
  9. Balázs Bálint
  10. László G Nagy
(2022)
Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom forming fungi (Agaricomycetes)
eLife 11:e71348.
https://doi.org/10.7554/eLife.71348

Share this article

https://doi.org/10.7554/eLife.71348

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