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PreprintCited by 14Fungal and yeast genetics researchFungal Biology and ApplicationsDevelopmental Biology and Gene Regulation

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Snowball: a novel gene family required for developmental patterning in fruiting bodies of mushroom-forming fungi (Agaricomycetes)

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Földi, Csenge, Merényi, Zsolt, Balázs, Bálint, Csernetics, Árpád, Miklovics, Nikolett, Wu, Hongli, Hegedüs, Botond, Virágh, Máté, Hou, Zhihao, Liu, Xiao-Bin, Galgóczy, László, Nagy, László G.·2023·mSystems
DOI 10.1101/2023.11.13.566867PMC PMC10949477

Preprint — published as 10.1128/msystems.01208-23 · Paper page

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Abstract

The morphogenesis of sexual fruiting bodies of fungi is a complex process determined by a genetically encoded program. Fruiting bodies reached the highest complexity levels in the Agaricomycetes, yet, the underlying genetics is currently poorly known. In this work, we functionally characterized a highly conserved unannotated gene termed snb1 , whose expression level increases rapidly during fruiting body initiation. According to phylogenetic analyses, orthologues of snb1 are present in almost all agaricomycetes and may represent a novel conserved gene family that plays a substantial role in fruiting body development. We disrupted snb1 using CRISPR/Cas9 in the agaricomycete model organism Coprinopsis cinerea. Snb1 deletion mutants formed unique, snowball-shaped, rudimentary fruiting bodies that could not differentiate caps, stipes and lamellae. We took advantage of this phenotype to study fruiting body differentiation using RNA-Seq analyses. This revealed differentially regulated genes and gene families that, based on wild-type RNA-Seq data, were upregulated early during development and showed tissue-specific expression, underscoring their potential role in differentiation. Taken together, the novel gene family of snb1 and the differentially expressed genes in the snb1 mutants provide valuable insights into the complex mechanisms underlying developmental patterning in the Agaricomycetes. Importance: Fruiting bodies of mushroom-forming fungi (Agaricomycetes) are complex multicellular structures, with a spatially and temporally integrated developmental program that is, however, currently poorly known. In this study we present a novel, conserved gene family, Snowball ( snb ), termed after the unique, differentiation-less fruiting body morphology of snb1 knockout strains in the model mushroom Coprinopsis cinerea. Snb is a hitherto unannotated gene that is highly conserved among agaricomycetes and encodes a protein of unknown function. A comparative transcriptomic analysis of the early developmental stages of differentiated wild-type and non-differentiated mutant fruiting bodies revealed conserved differentially expressed genes which may be related to tissue differentiation and developmental patterning fruiting body development.

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Metadata

Authors
Földi, C., Merényi, Z., Balázs, B., Csernetics, Á., Miklovics, N., Wu, H., Hegedüs, B., Virágh, M., Hou, Z., Liu, X.-B., Galgóczy, L., & Nagy, L. G.
Affiliations
  • University of Szeged (HU)
  • HUN-REN Szegedi Biológiai Kutatóközpont (HU)
Corresponding author
Nagy, László G.
ORCID
Venue
mSystems
Publisher
openRxiv
Published
2023-11-17
Volume
9
Issue
3
Pages
e0120823-e0120823
ISSN
2379-5077 (ISSN-L)
DOI
10.1101/2023.11.13.566867
PMC
PMC10949477
OpenAlex
W4391683639
Cited by
14
References
1
Citations by year
2026: 7 · 2025: 5 · 2024: 2
FWCI
1.81
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • mSystems (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • SZTE Publicatio Repozitórium (University of Szeged) (acceptedVersion, other-oa)
  • Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Hungarian Scientific Research Fund
  • Magyar Tudományos Akadémia (LP2019-13/2019)
  • Nemzeti Kutatási Fejlesztési és Innovációs Hivatal (OTKA 142188)
  • Nemzeti Kutatási, Fejlesztési és Innovaciós Alap (KDP-17-4, PALY-2021)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Health Sciences › Medicine › Pharmacology (medical) › Fungal Biology and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
fruiting body formation, Agaricomycetes, Coprinopsis cinerea, developmental patterning, histogenesis, gene family evolution, differentially expressed genes
MeSH terms
Agaricales, Ascomycota, Basidiomycota, Fungal Proteins, Phylogeny, Fruiting Bodies, Fungal

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