scholarly journals Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

2021 ◽  
Author(s):  
Laszlo G Nagy ◽  
Peter Jan Vonk ◽  
Markus Kunzler ◽  
Csenge Foldi ◽  
Mate Viragh ◽  
...  
Keyword(s):  
Cell Wall ◽  
Fruiting Body ◽  
Expression Patterns ◽  
Schizophyllum Commune ◽  
Gene Families ◽  
Second Phase ◽  
Fruiting Bodies ◽  
Body Development ◽  
Fruiting Body Development

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

scholarly journals Comparative Genomics and Transcriptomics To Analyze Fruiting Body Development in Filamentous Ascomycetes

Genetics ◽  
2019 ◽  
Vol 213 (4) ◽  
pp. 1545-1563 ◽  
Author(s):  
Ramona Lütkenhaus ◽  
Stefanie Traeger ◽  
Jan Breuer ◽  
Laia Carreté ◽  
Alan Kuo ◽  
...  
Keyword(s):  
Gene Expression ◽  
Fruiting Body ◽  
Molecular Mechanisms ◽  
Expression Patterns ◽  
Regulation Of Gene Expression ◽  
Comparative Transcriptomics ◽  
Fruiting Bodies ◽  
Body Development ◽  
Fruiting Body Development ◽  
Genes Encoding

Many filamentous ascomycetes develop three-dimensional fruiting bodies for production and dispersal of sexual spores. Fruiting bodies are among the most complex structures differentiated by ascomycetes; however, the molecular mechanisms underlying this process are insufficiently understood. Previous comparative transcriptomics analyses of fruiting body development in different ascomycetes suggested that there might be a core set of genes that are transcriptionally regulated in a similar manner across species. Conserved patterns of gene expression can be indicative of functional relevance, and therefore such a set of genes might constitute promising candidates for functional analyses. In this study, we have sequenced the genome of the Pezizomycete Ascodesmis nigricans, and performed comparative transcriptomics of developing fruiting bodies of this fungus, the Pezizomycete Pyronema confluens, and the Sordariomycete Sordaria macrospora. With only 27 Mb, the A. nigricans genome is the smallest Pezizomycete genome sequenced to date. Comparative transcriptomics indicated that gene expression patterns in developing fruiting bodies of the three species are more similar to each other than to nonsexual hyphae of the same species. An analysis of 83 genes that are upregulated only during fruiting body development in all three species revealed 23 genes encoding proteins with predicted roles in vesicle transport, the endomembrane system, or transport across membranes, and 13 genes encoding proteins with predicted roles in chromatin organization or the regulation of gene expression. Among four genes chosen for functional analysis by deletion in S. macrospora, three were shown to be involved in fruiting body formation, including two predicted chromatin modifier genes.

scholarly journals SdeK Is Required for Early Fruiting Body Development in Myxococcus xanthus

1998 ◽  
Vol 180 (17) ◽  
pp. 4628-4637 ◽  
Author(s):  
Anthony G. Garza ◽  
Jeffrey S. Pollack ◽  
Baruch Z. Harris ◽  
Albert Lee ◽  
Ingrid M. Keseler ◽  
...  
Keyword(s):  
Dna Sequence ◽  
Fruiting Body ◽  
Developmental Process ◽  
Transcriptional Start Site ◽  
Expression Patterns ◽  
Myxococcus Xanthus ◽  
Predicted Amino Acid Sequence ◽  
Developmental Program ◽  
Body Development ◽  
Fruiting Body Development

ABSTRACT Myxococcus xanthus cells carrying the Ω4408 Tn5lac insertion at the sde locus show defects in fruiting body development and sporulation. Our analysis ofsde expression patterns showed that this locus is induced early in the developmental program (0 to 2 h) and that expression increases approximately fivefold after 12 h of development. Further studies showed that expression of sde is induced as growing cells enter stationary phase, suggesting that activation of thesde locus is not limited to the developmental process. Because the peak levels of sde expression in both ansde + and an sde mutant background were similar, we conclude that the sde locus is not autoregulated. Characterization of the sde locus by DNA sequence analysis indicated that the Ω4408 insertion occurred within the sdeK gene. Primer extension analyses localized the 5′ end of sde transcript to a guanine nucleotide 307 bp upstream of the proposed start for the SdeK coding sequence. The DNA sequence in the −12 and −24 regions upstream of the sdetranscriptional start site shows similarity to the ς54family of promoters. The results of complementation studies suggest that the defects in development and sporulation caused by the Ω4408 insertion are due to an inactivation of sdeK. The predicted amino acid sequence of SdeK was found to have similarity to the sequences of the histidine protein kinases of two-component regulatory systems. Based on our results, we propose that SdeK may be part of a signal transduction pathway required for the activation and propagation of the early developmental program.

scholarly journals Transcript Profiling Reveals Novel Marker Genes Involved in Fruiting Body Formation in Tuber borchii

2005 ◽  
Vol 4 (9) ◽  
pp. 1599-1602 ◽  
Author(s):  
Silvia Gabella ◽  
Simona Abbà ◽  
Sebastien Duplessis ◽  
Barbara Montanini ◽  
Francis Martin ◽  
...  
Keyword(s):  
Fruiting Body ◽  
Marker Genes ◽  
Fruiting Bodies ◽  
Fruiting Body Formation ◽  
Tuber Borchii ◽  
Body Formation ◽  
Physiological Processes ◽  
Body Development ◽  
Fruiting Body Development ◽  
Two Stages

ABSTRACT cDNA arrays were used to explore mechanisms controlling fruiting body development in the truffle Tuber borchii. Differences in gene expression were higher between reproductive and vegetative stage than between two stages of fruiting body maturation. We suggest hypotheses about the importance of various physiological processes during the development of fruiting bodies.

scholarly journals σ54 Enhancer Binding Proteins and Myxococcus xanthus Fruiting Body Development

2004 ◽  
Vol 186 (13) ◽  
pp. 4361-4368 ◽  
Author(s):  
Jimmy S. Jakobsen ◽  
Lars Jelsbak ◽  
Lotte Jelsbak ◽  
Roy D. Welch ◽  
Craig Cummings ◽  
...  
Keyword(s):  
Fruiting Body ◽  
Binding Proteins ◽  
Myxococcus Xanthus ◽  
Fruiting Bodies ◽  
Knockout Mutant ◽  
Developmentally Regulated ◽  
Enhancer Binding Proteins ◽  
Developmental Program ◽  
Body Development ◽  
Fruiting Body Development

ABSTRACT A search of the M1genome sequence, which includes 97% of the Myxococcus xanthus genes, identified 53 sequence homologs of σ54-dependent enhancer binding proteins (EBPs). A DNA microarray was constructed from the M1genome that includes those homologs and 318 other M. xanthus genes for comparison. To screen the developmental program with this array, an RNA extract from growing cells was compared with one prepared from developing cells at 12 h. Previous reporter studies had shown that M. xanthus has initiated development and has begun to express many developmentally regulated genes by 12 h. The comparison revealed substantial increases in the expression levels of 11 transcription factors that may respond to environmental stimuli. Six of the 53 EBP homologs were expressed at significantly higher levels at 12 h of development than during growth. Three were previously unknown genes, and they were inactivated to look for effects on fruiting body development. One knockout mutant produced fruiting bodies of abnormal shape that depended on the composition of the medium.

scholarly journals The Myxococcus xanthus Nla4 Protein Is Important for Expression of Stringent Response-Associated Genes, ppGpp Accumulation, and Fruiting Body Development

2007 ◽  
Vol 189 (23) ◽  
pp. 8474-8483 ◽  
Author(s):  
Faisury Ossa ◽  
Michelle E. Diodati ◽  
Nora B. Caberoy ◽  
Krista M. Giglio ◽  
Mick Edmonds ◽  
...  
Keyword(s):  
Fruiting Body ◽  
Expression Patterns ◽  
Myxococcus Xanthus ◽  
Stringent Response ◽  
Fruiting Body Formation ◽  
Body Development ◽  
Normal Expression ◽  
Fruiting Body Development ◽  
Coordinated Expression ◽  
Low Levels

ABSTRACT Changes in gene expression are important for the landmark morphological events that occur during Myxococcus xanthus fruiting body development. Enhancer binding proteins (EBPs), which are transcriptional activators, play prominent roles in the coordinated expression of developmental genes. A mutation in the EBP gene nla4 affects the timing of fruiting body formation, the morphology of mature fruiting bodies, and the efficiency of sporulation. In this study, we showed that the nla4 mutant accumulates relatively low levels of the stringent nucleotide ppGpp. We also found that the nla4 mutant is defective for early developmental events and for vegetative growth, phenotypes that are consistent with a deficiency in ppGpp accumulation. Further studies revealed that nla4 cells produce relatively low levels of GTP, a precursor of RelA-dependent synthesis of (p)ppGpp. In addition, the normal expression patterns of all stringent response-associated genes tested, including the M. xanthus ppGpp synthetase gene relA, are altered in nla4 mutant cells. These findings indicate that Nla4 is part of regulatory pathway that is important for mounting a stringent response and for initiating fruiting body development.

scholarly journals Nla18, a Key Regulatory Protein Required for Normal Growth and Development of Myxococcus xanthus

2006 ◽  
Vol 188 (5) ◽  
pp. 1733-1743 ◽  
Author(s):  
Michelle E. Diodati ◽  
Faisury Ossa ◽  
Nora B. Caberoy ◽  
Ivy R. Jose ◽  
Wataru Hiraiwa ◽  
...  
Keyword(s):  
Gene Expression ◽  
Gene Regulation ◽  
Fruiting Body ◽  
Vegetative Growth ◽  
Growth And Development ◽  
Expression Patterns ◽  
Myxococcus Xanthus ◽  
Body Development ◽  
Fruiting Body Development ◽  
Mutant Cells

ABSTRACT NtrC-like activators regulate the transcription of a wide variety of adaptive genes in bacteria. Previously, we demonstrated that a mutation in the ntrC-like activator gene nla18 causes defects in fruiting body development in Myxococcus xanthus. In this report, we describe the effect that nla18 inactivation has on gene expression patterns during development and vegetative growth. Gene expression in nla18 mutant cells is altered in the early stages of fruiting body development. Furthermore, nla18 mutant cells are defective for two of the earliest events in development, production of the intracellular starvation signal ppGpp and production of A-signal. Taken together, these results indicate that the developmental program in nla18 mutant cells goes awry very early. Inactivation of nla18 also causes a dramatic decrease in the vegetative growth rate of M. xanthus cells. DNA microarray analysis revealed that the vegetative expression patterns of more than 700 genes are altered in nla18 mutant cells. Genes coding for putative membrane and membrane-associated proteins are among the largest classes of genes whose expression is altered by nla18 inactivation. This result is supported by our findings that the profiles of membrane proteins isolated from vegetative nla18 mutant and wild-type cells are noticeably different. In addition to genes that code for putative membrane proteins, nla18 inactivation affects the expression of many genes that are likely to be important for protein synthesis and gene regulation. Our data are consistent with a model in which Nla18 controls vegetative growth and development by activating the expression of genes involved in gene regulation, translation, and membrane structure.

scholarly journals Discovery of microRNA-like RNAs during early fruiting body development in the model mushroom Coprinopsis cinerea

2018 ◽  
Author(s):  
Amy Yuet Ting Lau ◽  
Xuanjin Cheng ◽  
Chi Keung Cheng ◽  
Wenyan Nong ◽  
Man Kit Cheung ◽  
...  
Keyword(s):  
Fruiting Body ◽  
Developmental Stages ◽  
Expression Patterns ◽  
Regulation Of Gene Expression ◽  
Evolutionary Relationship ◽  
Mirna Biogenesis ◽  
Coprinopsis Cinerea ◽  
Stem Loop ◽  
Body Development ◽  
Fruiting Body Development

AbstractCoprinopsis cinerea is a model mushroom particularly suited to study fungal fruiting body development and the evolution of multicellularity in fungi. While microRNAs (miRNAs) are extensively studied in animals and plants for their essential roles in post-transcriptional regulation of gene expression, miRNAs in fungi are less well characterized and their potential roles in controlling mushroom development remain unknown. To identify miRNA-like RNAs (milRNAs) in C. cinerea and explore their expression patterns during the early developmental transition of mushroom development, small RNA libraries of vegetative mycelium and primordium were generated and putative milRNA candidates were identified following the standards of miRNA prediction in animals and plants. Two out of 22 novel predicted milRNAs, cci-milR-12c and cci-milR-13e-5p, were validated by northern blot and stem-loop reverse transcription real-time PCR. Cci-milR-12c was differentially expressed whereas the expression levels of cci-milR-13e-5p were similar in the two developmental stages. Target prediction of the validated milRNAs resulted in genes associated with fruiting body development, including pheromone, hydrophobin, cytochrome P450, and protein kinase. Besides, essential genes for miRNA biogenesis, including three coding for Dicer-like (DCL), two for Argonaute-like (AGO-like) and one for quelling deficient-2 (QDE-2) proteins, were identified in the C. cinerea genome. Phylogenetic analysis showed that the DCL and AGO-like proteins of C. cinerea were more closely related to those in other basidiomycetes and ascomycetes than to animals and plants. Taken together, our findings provided the first evidence of milRNAs in the model mushroom and their potential roles in regulating fruiting body development. Information on the evolutionary relationship of milRNA biogenesis proteins across kingdoms has also provided new insights into further functional and evolutionary studies of miRNAs.

scholarly journals EspC Is Involved in Controlling the Timing of Development in Myxococcus xanthus

2005 ◽  
Vol 187 (14) ◽  
pp. 5029-5031 ◽  
Author(s):  
Bongsoo Lee ◽  
Penelope I. Higgs ◽  
David R. Zusman ◽  
Kyungyun Cho
Keyword(s):  
Fruiting Body ◽  
Type Strain ◽  
Wild Type Strain ◽  
Myxococcus Xanthus ◽  
Null Mutation ◽  
Fruiting Bodies ◽  
Wild Type ◽  
Body Development ◽  
Fruiting Body Development

ABSTRACT The espC null mutation caused accelerated aggregation and formation of tiny fruiting bodies surrounded by spores, which were also observed in the espA mutant and in CsgA-overproducing cells in Myxococcus xanthus. In addition, the espC mutant appeared to produce larger amounts of the complementary C-signal than the wild-type strain. These findings suggest that EspC is involved in controlling the timing of fruiting body development in M. xanthus.

scholarly journals Distribution, evolution and expression of GATA-TFs provide new insights into their functions in light response and fruiting body development of Tolypocladium guangdongense

PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9784
Author(s):  
Chenghua Zhang ◽  
Gangzheng Wang ◽  
Wangqiu Deng ◽  
Taihui Li
Keyword(s):  
Fruiting Body ◽  
Developmental Stages ◽  
Special Functions ◽  
Expression Patterns ◽  
Protein Structures ◽  
Light Response ◽  
Biological Processes ◽  
Expression Levels ◽  
Body Development ◽  
Fruiting Body Development

Background Fungal GATA-type transcription factors (GATA-TFs) are a class of transcriptional regulators involved in various biological processes. However, their functions are rarely analyzed systematically, especially in edible or medicinal fungi, such as Tolypocladium guangdongense, which has various medicinal and food safety properties with a broad range of potential applications in healthcare products and the pharmaceutical industry. Methods GATA-TFs in T. guangdongense (TgGATAs) were identified using InterProScan. The type, distribution, and gene structure of TgGATAs were analyzed by genome-wide analyses. A phylogenetic tree was constructed to analyze their evolutionary relationships using the neighbor-joining (NJ) method. To explore the functions of GATA-TFs, conserved domains were analyzed using MEME, and cis-elements were predicted using the PlantCARE database. In addition, the expression patterns of TgGATAs under different light conditions and developmental stages were studied using qPCR. Results Seven TgGATAs were identified. They were randomly distributed on four chromosomes and contained one to four exons. Phylogenetic analysis indicated that GATA-TFs in each subgroup are highly conserved, especially for GATA1 to GATA5. Intron distribution analyses suggested that GATA1 and GATA3 possessed the most conserved gene structures. Light treatments induced the expression levels of TgGATA1 and TgGATA5-7, but the expression levels varied depending on the duration of illumination. The predicted protein structures indicate that TgGATA1 and TgGATA2 possess typical light-responsive domains and may function as photoreceptors to regulate downstream biological processes. TgGATA3 and TgGATA5 may be involved in nitrogen metabolism and siderophore biosynthesis, respectively. TgGATA6 and TgGATA7 possess unique Zn finger loop sequences, suggesting that they may have special functions. Furthermore, gene expression analysis indicated that TgGATA1 (WC1) was notably involved in mycelial color transformation, while other genes were involved in fruiting body development to some extent. These results provide valuable information to further explore the mechanisms through which TgGATAs are regulated during fruiting body development.

scholarly journals Whole-Genome and Transcriptome Sequencing of Phlebopus portentosus Reveals Its Associated Ectomycorrhizal Niche and Conserved Pathways Involved in Fruiting Body Development

2021 ◽  
Vol 12 ◽  
Author(s):  
Jia-Ning Wan ◽  
Yan Li ◽  
Ting Guo ◽  
Guang-Yan Ji ◽  
Shun-Zhen Luo ◽  
...  
Keyword(s):  
Cell Wall ◽  
Plant Cell ◽  
Fruiting Body ◽  
Transcriptome Sequencing ◽  
Plant Cell Wall ◽  
Expression Profiles ◽  
Mapk Signaling ◽  
Body Development ◽  
A Genome ◽  
Fruiting Body Development

Phlebopus portentosus (Berk. and Broome) Boedijin, a widely consumed mushroom in China and Thailand, is the first species in the order Boletaceae to have been industrially cultivated on a large scale. However, to date, the lignocellulose degradation system and molecular basis of fruiting body development in P. portentosus have remained cryptic. In the present study, genome and transcriptome sequencing of P. portentosus was performed during the mycelium (S), primordium (P), and fruiting body (F) stages. A genome of 32.74 Mb with a 48.92% GC content across 62 scaffolds was obtained. A total of 9,464 putative genes were predicted from the genome, of which the number of genes related to plant cell wall-degrading enzymes was much lower than that of some saprophytic mushrooms with specific ectomycorrhizal niches. Principal component analysis of RNA-Seq data revealed that the gene expression profiles at all three stages were different. The low expression of plant cell wall-degrading genes also confirmed the limited ability to degrade lignocellulose. The expression profiles also revealed that some conserved and specific pathways were enriched in the different developmental stages of P. portentosus. Starch and sucrose metabolic pathways were enriched in the mycelium stage, while DNA replication, the proteasome and MAPK signaling pathways may be associated with maturation. These results provide a new perspective for understanding the key pathways and hub genes involved in P. portentosus development.

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