The<i>Coprinopsis cinerea</i>Tup1 homologue Cag1 is required for gill formation during fruiting body morphogenesis

Masuda, Ryo; Iguchi, Naoki; Tukuta, Kooki; Nagoshi, Takahiro; Kemuriyama, Kazuki; Muraguchi, Hajime

doi:10.1242/bio.021246

Cited by 14 publications

(13 citation statements)

References 38 publications

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“…Both wc2 and pacC are conserved in both ascomycetes and basidiomycetes and except for hmg1 (F. velutipes), lfc1 (F. velutipes), pdd1 (F. velutipes), pcc1 (C. cinerea and P. ostreatus) and zfc7 (S. commune) all characterized transcription factors are at least conserved in mushroom-forming fungi. Cag1 ( C. cinerea protein ID: 466216) and Cc.Tup1 ( C. cinerea protein ID: 369655) of C. cinerea are further examples of highly conserved transcription factors(Masuda et al 2016). They are homologs of the highly conserved general transcriptional co-repressor Tup1 of S. cerevisiae , which can form repressive complexes with a wide range of sequence-specific transcription factors.…”

Section: Results: Developmentally Expressed Gene Classes In the Agari...mentioning

confidence: 99%

“…They are homologs of the highly conserved general transcriptional co-repressor Tup1 of S. cerevisiae, which can form repressive complexes with a wide range of sequence-specific transcription factors. Deletion of Cag1 resulted in a cap-growthless phenotype, which, upon closer inspection turned out to be caused by developmental defects of gills (Masuda et al 2016). However, the expression patterns are generally not conserved during fruiting body development (Almási et al 2019;Krizsán et al 2019).…”

Section: Transcriptional Regulators 451 Transcription Factorsmentioning

confidence: 99%

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Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

Nagy

Vonk

Künzler

et al. 2021

Preprint

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Fruiting bodies of mushroom-forming fungi (Agaricomycetes) are among the most complex structures produced by fungi. Unlike vegetative hyphae, fruiting bodies grow determinately and follow a genetically encoded developmental program that orchestrates tissue differentiation, growth and sexual sporulation. In spite of more than a century of research, our understanding of the molecular details of fruiting body morphogenesis is limited and a general synthesis on the genetics of this complex process is lacking. In this paper, we aim to comprehensively identify conserved genes related to fruiting body morphogenesis and distill novel functional hypotheses for functionally poorly characterized genes. As a result of this analysis, we report 921 conserved developmentally expressed gene families, only a few dozens of which have previously been reported in fruiting body development. Based on literature data, conserved expression patterns and functional annotations, we provide informed hypotheses on the potential role of these gene families in fruiting body development, yielding the most complete description of molecular processes in fruiting body morphogenesis to date. We discuss genes related to the initiation of fruiting, differentiation, growth, cell surface and cell wall, defense, transcriptional regulation as well as signal transduction. Based on these data we derive a general model of fruiting body development, which includes an early, proliferative phase that is mostly concerned with laying out the mushroom body plan (via cell division and differentiation), and a second phase of growth via cell expansion as well as meiotic events and sporulation. Altogether, our discussions cover 1480 genes of Coprinopsis cinerea, and their orthologs in Agaricus bisporus, Cyclocybe aegerita, Armillaria ostoyae, Auriculariopsis ampla, Laccaria bicolor, Lentinula edodes, Lentinus tigrinus, Mycena kentingensis, Phanerochaete chrysosporium, Pleurotus ostreatus, and Schizophyllum commune, providing functional hypotheses for ~10% of genes in the genomes of these species. Although experimental evidence for the role of these genes will need to be established in the future, our data provide a roadmap for guiding functional analyses of fruiting related genes in the Agaricomycetes. We anticipate that the gene compendium presented here, combined with developments in functional genomics approaches will contribute to uncovering the genetic bases of one of the most spectacular multicellular developmental processes in fungi. Key words: functional annotation; comparative genomics; cell wall remodeling; development; fruiting body morphogenesis; mushroom; transcriptome

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Section: Results: Developmentally Expressed Gene Classes In the Agari...mentioning

confidence: 99%

Section: Transcriptional Regulators 451 Transcription Factorsmentioning

confidence: 99%

Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

Nagy

Vonk

Künzler

et al. 2021

Preprint

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“…Known structural genes include ones coding for hydrophobins (Lugones et al ., ; Wösten et al ., ; Bayry et al ., ), lectins (Cooper et al ., ; Boulianne et al ., ; Hassan et al ., ) and several cell wall chitin and glucan‐active CAZymes (Wessels, ; Fukuda et al ., ; Konno & Sakamoto, ; Sakamoto et al ., ), and probably include genes for cerato‐platanins, which are expansin‐like proteins (Sipos et al ., ; Krizsán et al ., ), among others. Regulators of fruiting body development have been characterized in several species, in particular in Coprinopsis cinerea (Stajich et al ., ; Cheng et al ., ; de Sena‐Tomas et al ., ; Muraguchi et al ., ; Masuda et al ., ) and S. commune (Ohm et al ., , ; Pelkmans et al ., ). Despite advances in this field, several aspects of fruiting body development are poorly known, including, for example, what genes have conserved developmental roles across fruiting body‐forming fungi or how cell–cell communication is orchestrated in developing fruiting bodies.…”

Section: Introductionmentioning

confidence: 99%

Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae

et al. 2019

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Summary Agaricomycetes are fruiting body‐forming fungi that produce some of the most efficient enzyme systems to degrade wood. Despite decades‐long interest in their biology, the evolution and functional diversity of both wood‐decay and fruiting body formation are incompletely known. We performed comparative genomic and transcriptomic analyses of wood‐decay and fruiting body development in Auriculariopsis ampla and Schizophyllum commune (Schizophyllaceae), species with secondarily simplified morphologies, an enigmatic wood‐decay strategy and weak pathogenicity to woody plants. The plant cell wall‐degrading enzyme repertoires of Schizophyllaceae are transitional between those of white rot species and less efficient wood‐degraders such as brown rot or mycorrhizal fungi. Rich repertoires of suberinase and tannase genes were found in both species, with tannases restricted to Agaricomycetes that preferentially colonize bark‐covered wood, suggesting potential complementation of their weaker wood‐decaying abilities and adaptations to wood colonization through the bark. Fruiting body transcriptomes revealed a high rate of divergence in developmental gene expression, but also several genes with conserved expression patterns, including novel transcription factors and small‐secreted proteins, some of the latter which might represent fruiting body effectors. Taken together, our analyses highlighted novel aspects of wood‐decay and fruiting body development in an important family of mushroom‐forming fungi.

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“…For example, Arp9 , Pcc1 , and Ubc2 are involved in clamp cell formation and are essential for fruiting initiation [ 10 , 11 , 12 ]. Cag1 is preferentially expressed in gill trama tissue cells and is involved in the formation of the pileus during the development of primordia [ 13 ]. Eln2 participates in the development of primordia and stipe elongation [ 14 ].…”

Section: Introductionmentioning

confidence: 99%

MAPK CcSakA of the HOG Pathway Is Involved in Stipe Elongation during Fruiting Body Development in Coprinopsis cinerea

Zhao

Yuan

Chen

et al. 2022

JoF

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Mitogen-activated protein kinase (MAPK) pathways, such as the high-osmolarity glycerol mitogen-activated protein kinase (HOG) pathway, are evolutionarily conserved signaling modules responsible for transmitting environmental stress signals in eukaryotic organisms. Here, we identified the MAPK homologue in the HOG pathway of Coprinopsis cinerea, which was named CcSakA. Furthermore, during the development of the fruiting body, CcSakA was phosphorylated in the fast elongating apical part of the stipe, which meant that CcSakA was activated in the apical elongating stipe region of the fruiting body. The knockdown of CcSakA resulted in a shorter stipe of the fruiting body compared to the control strain, and the expression of phosphomimicking mutant CcSakA led to a longer stipe of the fruiting body compared to the control strain. The chitinase CcChiE1, which plays a key role during stipe elongation, was downregulated in the CcSakA knockdown strains and upregulated in the CcSakA phosphomimicking mutant strains. The results indicated that CcSakA participated in the elongation of stipes in the fruiting body development of C. cinerea by regulating the expression of CcChiE1. Analysis of the H2O2 concentration in different parts of the stipe showed that the oxidative stress in the elongating part of the stipe was higher than those in the non-elongating part. The results indicated that CcSakA of the HOG pathway may be activated by oxidative stress. Our results demonstrated that the HOG pathway transmits stress signals and regulates the expression of CcChiE1 during fruiting body development in C. cinerea.

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TheCoprinopsis cinereaTup1 homologue Cag1 is required for gill formation during fruiting body morphogenesis

Cited by 14 publications

References 38 publications

Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae

MAPK CcSakA of the HOG Pathway Is Involved in Stipe Elongation during Fruiting Body Development in Coprinopsis cinerea

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