Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea

Fruiting bodies of mushroom-forming fungi (Agaricomycetes) are complex multicellular structures whose formation is regulated by a developmental program that dynamically responds to environmental changes, such as light intensity. However, the genetic architecture and regulation of this developmental...

Full description

Saved in:
Bibliographic Details
Main Authors: Benedek Szathmári, Balázs Bálint, Botond Hegedüs, Máté Virágh, Zhihao Hou, Xiao-Bin Liu, Hongli Wu, Csenge Földi, Julien Gagneur, Johann Promeuschel, Árpád Csernetics, László G. Nagy
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Fungal Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/ffunb.2025.1633301/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849245447970881536
author Benedek Szathmári
Balázs Bálint
Botond Hegedüs
Máté Virágh
Zhihao Hou
Zhihao Hou
Xiao-Bin Liu
Hongli Wu
Csenge Földi
Julien Gagneur
Julien Gagneur
Johann Promeuschel
Árpád Csernetics
László G. Nagy
László G. Nagy
author_facet Benedek Szathmári
Balázs Bálint
Botond Hegedüs
Máté Virágh
Zhihao Hou
Zhihao Hou
Xiao-Bin Liu
Hongli Wu
Csenge Földi
Julien Gagneur
Julien Gagneur
Johann Promeuschel
Árpád Csernetics
László G. Nagy
László G. Nagy
author_sort Benedek Szathmári
collection DOAJ
description Fruiting bodies of mushroom-forming fungi (Agaricomycetes) are complex multicellular structures whose formation is regulated by a developmental program that dynamically responds to environmental changes, such as light intensity. However, the genetic architecture and regulation of this developmental program are poorly known. Here, we characterize a novel Pumilio family gene, ort2, which influences fruiting body development, particularly the formation of dark stipes, a light-dependent alternative developmental trajectory. Phylogenetic analysis of this RNA-binding protein family in fungi revealed a distinct subfamily structure, with high conservation of each subfamily within Agaricomycetes. Reverse genetics experiments in the model species Coprinopsis cinerea revealed that ort2 disruptants produced fruiting bodies, but were deficient in dark stipe formation, whereas the overexpression mutants produced significantly more dark stipes. The gene was named after Orthrus, the two-headed dog of classical mythology, based on rare but reproducible branching fruiting body phenotypes observed upon overexpression. Our findings reveal fruiting-related functions for ort2, a novel conserved RNA-binding protein, and may serve as a novel entry point for understanding the molecular basis of dark stipe development.
format Article
id doaj-art-48860181fcf04a71924fdfc85b5f1e12
institution Kabale University
issn 2673-6128
language English
publishDate 2025-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Fungal Biology
spelling doaj-art-48860181fcf04a71924fdfc85b5f1e122025-08-20T03:58:49ZengFrontiers Media S.A.Frontiers in Fungal Biology2673-61282025-07-01610.3389/ffunb.2025.16333011633301Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinereaBenedek Szathmári0Balázs Bálint1Botond Hegedüs2Máté Virágh3Zhihao Hou4Zhihao Hou5Xiao-Bin Liu6Hongli Wu7Csenge Földi8Julien Gagneur9Julien Gagneur10Johann Promeuschel11Árpád Csernetics12László G. Nagy13László G. Nagy14Synthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungaryDoctoral School of Biology, Faculty of Science and Informatics, University of Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySchool of Computation, Information and Technology, Technical University of Munich, Garching, GermanyMunich Center for Machine Learning, Munich, GermanySchool of Computation, Information and Technology, Technical University of Munich, Garching, GermanySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungarySynthetic and Systems Biology Unit, Institute of Biochemistry, HUN-REN Biological Research Centre Szeged, Szeged, HungaryKorea University, Seoul, Republic of KoreaFruiting bodies of mushroom-forming fungi (Agaricomycetes) are complex multicellular structures whose formation is regulated by a developmental program that dynamically responds to environmental changes, such as light intensity. However, the genetic architecture and regulation of this developmental program are poorly known. Here, we characterize a novel Pumilio family gene, ort2, which influences fruiting body development, particularly the formation of dark stipes, a light-dependent alternative developmental trajectory. Phylogenetic analysis of this RNA-binding protein family in fungi revealed a distinct subfamily structure, with high conservation of each subfamily within Agaricomycetes. Reverse genetics experiments in the model species Coprinopsis cinerea revealed that ort2 disruptants produced fruiting bodies, but were deficient in dark stipe formation, whereas the overexpression mutants produced significantly more dark stipes. The gene was named after Orthrus, the two-headed dog of classical mythology, based on rare but reproducible branching fruiting body phenotypes observed upon overexpression. Our findings reveal fruiting-related functions for ort2, a novel conserved RNA-binding protein, and may serve as a novel entry point for understanding the molecular basis of dark stipe development.https://www.frontiersin.org/articles/10.3389/ffunb.2025.1633301/fullfruiting body formationdark stipeRNA-binding proteinsPumiliolanguage model
spellingShingle Benedek Szathmári
Balázs Bálint
Botond Hegedüs
Máté Virágh
Zhihao Hou
Zhihao Hou
Xiao-Bin Liu
Hongli Wu
Csenge Földi
Julien Gagneur
Julien Gagneur
Johann Promeuschel
Árpád Csernetics
László G. Nagy
László G. Nagy
Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
Frontiers in Fungal Biology
fruiting body formation
dark stipe
RNA-binding proteins
Pumilio
language model
title Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
title_full Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
title_fullStr Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
title_full_unstemmed Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
title_short Orthrus: a Pumilio-family gene involved in fruiting body and dark stipe development in Coprinopsis cinerea
title_sort orthrus a pumilio family gene involved in fruiting body and dark stipe development in coprinopsis cinerea
topic fruiting body formation
dark stipe
RNA-binding proteins
Pumilio
language model
url https://www.frontiersin.org/articles/10.3389/ffunb.2025.1633301/full
work_keys_str_mv AT benedekszathmari orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT balazsbalint orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT botondhegedus orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT mateviragh orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT zhihaohou orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT zhihaohou orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT xiaobinliu orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT hongliwu orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT csengefoldi orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT juliengagneur orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT juliengagneur orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT johannpromeuschel orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT arpadcsernetics orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT laszlognagy orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea
AT laszlognagy orthrusapumiliofamilygeneinvolvedinfruitingbodyanddarkstipedevelopmentincoprinopsiscinerea