Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom-forming fungi (Agaricomycetes)

Abstract

Multicellularity has been one of the most important innovations in the history of life. The role of gene regulatory changes in driving transitions to multicellularity is being increasingly recognized; however, factors influencing gene expression patterns are poorly known in many clades. Here we compared the developmental transcriptomes of complex multicellular fruiting bodies of eight Agaricomycetes and Cryptococcus neoformans, a closely related human pathogen with a simple morphology. In-depth analysis in Pleurotus ostreatus revealed that allele-specific expression, natural antisense transcripts and developmental gene expression, but not RNA editing or a 'developmental hourglass' act in concert to shape its transcriptome during fruiting body development. We found that transcriptional patterns of genes strongly depend on their evolutionary ages. Young genes showed more developmental and allele-specific expression variation, possibly because of weaker evolutionary constraint, suggestive of non-adaptive expression variance in fruiting bodies. These results prompted us to define a set of conserved genes specifically regulated only during complex morphogenesis by excluding young genes and accounting for deeply conserved ones shared with species showing simple sexual development. Analysis of the resulting gene set revealed evolutionary and functional associations with complex multicellularity, which allowed us to speculate they are involved in complex multicellular morphogenesis of mushroom fruiting bodies.

Taxonomic vs genomic fungi: contrasting evolutionary loss of protistan genomic heritage and emergence of fungal novelties

“…All-vs-all similarity searches of the 123 proteomes were performed with MMseqs2 51 using three iterations, with sensitivity set to 6.5, max-seqs to 15,000, e-profile set to 0.001, a preliminary coverage threshold set to 0.2, and an e-value threshold set to 1e -4 . We then performed an asymmetric coverage filtering (requiring 20% coverage for the longer and 80% for the shorter protein) and Markov clustering with an inflation parameter 2.0 52 as described previously 53 . After clustering, we removed contaminating proteins from gene families following the logic of Richter et al 47 .…”

Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes

“…Hypothetical genes are often fungal or lineage specific, and thus have often been less well characterized than deeply conserved genes at higher taxonomic levels. Although greater degrees of transcriptional divergence of hypothetical genes may be attributable to neutrally arising expression variation widely observed in young genes because of weaker evolutionary constraint ( 56 ), our systemic knockout studies for hypothetical genes demonstrated that these hypothetical genes have evolved to be necessary for successful sexual development, showing significant shifts in their expression levels in certain groups of fungi.…”

“…It was shown that deeply conserved genes (“old genes”), as well as newly emerged genes (“young genes”) tend to be expressed during specific developmental stages in fungi, playing important roles in sculpting fruiting body morphologies ( 56 ). To assess the ages of the annotated genes in the F. graminearum and N. crassa genomes, we sorted hypothetical genes and genes with predicted functional domains (henceforth referred as “functional genes”) using a phylostratigraphic approach, in which ages of the phylogenetically classified genes were assigned based on the set of species that share orthologous genes.…”

The Phylotranscriptomic Hourglass Pattern in Fungi: An Updated Model

“…Many comparative studies have been conducted to clarify the driven factors in fungal morphogenesis and multicellularity construction (Kiss et al 2019; Krizsán et al 2019; Varga et al 2019; Merényi et al 2020; Miyauchi et al 2020; Virágh et al 2022). Questions have been raised on the robustness of the hourglass model in fruiting body development in some fungal clades (Merényi et al 2022).…”

“…Questions have been raised on the robustness of the hourglass model in fruiting body development in some fungal clades (Merényi et al 2022).…”