Lessons on fruiting body morphogenesis from genomes and transcriptomes of Agaricomycetes

Abstract

Fruiting bodies (sporocarps, sporophores or basidiomata) 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 their growth, tissue differentiation and sexual sporulation. In spite of more than a century of research, our understanding of the molecular details of fruiting body morphogenesis is still limited and a general synthesis on the genetics of this complex process is lacking. In this paper, we aim at a comprehensive identification of conserved genes related to fruiting body morphogenesis and distil novel functional hypotheses for functionally poorly characterised ones. As a result of this analysis, we report 921 conserved developmentally expressed gene families, only a few dozens of which have previously been reported to be involved in fruiting body development. Based on literature data, conserved expression patterns and functional annotations, we provide 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, defence, 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 1 480 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.

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

“…However, due to their rapid evolution and the lack of more precise functional data, it is difficult to infer their functions with more specificity. Functionally poorly known genes -This category mainly includes genes with predicted functions that cannot be easily linked to fruiting body formation (28). We detected 43 DEGs in this category, of which 18 are downregulated and 25 are upregulated.…”

“…To better interpret the functions of DEGs, we classified them into 18 manually curated functional categories defined for conserved development-related genes, which cover 1,410 genes of C. cinerea (28). In this way, 205 DEGs were classified into fourteen functional categories (Fig.…”

“…Basic metabolism and acetyl-CoA -This functional group includes several metabolic pathways that directly or indirectly converge on increased acetyl-CoA production, which is the central intermediate during the metabolism of non-fermentable carbon sources and is a building block of biological membranes (44). It was speculated that developmental regulation of genes in this category supplies acetyl-CoA for cell membrane assembly during rapid cell expansion in the growing fruiting body (28). Of the 20 DEGs in this category, 5 were downregulated in the Δsnb1.…”

“…However, there is currently a large gap between -omics studies and genetic analysis of developmental genes. While the former can identify hundreds to thousands of developmentally regulated genes, functional analysis of these is lagging behind, with orders of magnitudes fewer genes with a known function, in any species (28). Uncovering the precise function of these genes could fill the gaps in our understanding of the complex molecular networks underlying fruiting body development.…”

“…The latest developmental-omics studies identified hundreds of unannotated genes in fruiting body transcriptomes, many of which displayed considerable sequence conservation and even showed conserved expression patterns. A recent analysis of twelve mushroom-forming species found that a large proportion of conserved developmentally regulated genes is, actually, unannotated and that the genome of Coprinopsis cinerea alone contains 158 such families (28). On the other hand, less than a handful of them have been functionally characterized in mushroom-forming fungi.…”