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Krizsan, K.

Publications and source records attributed to Krizsan, K..

6 recordsLinked to original sources

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

Fungi are among the most ecologically important heterotrophs that have radiated into most niches on Earth and fulfil key ecological services. However, despite intense interest in their origins, major genomic trends characterising the evolutionary route from a unicellular opisthokont ancestor to derived multicellular fungi remain poorly known. Here, we reconstructed gene family evolution across 123 genomes of fungi and relatives and show that a dominant trend in early fungal evolution has been the gradual shedding of protist genes and highly episodic innovation via gene duplication. We find that the gene content of early-diverging fungi is protist-like in many respects, owing to the conservation of protist genes in early fungi. While gene loss has been constant and gradual during early fungal evolution, our reconstructions show that gene innovation showed two peaks. Gene groups with the largest contribution to genomic change included extracellular proteins, transcription factors, as well as ones linked to the coordination of nutrient uptake with growth, highlighting the transition to a sessile osmotrophic feeding strategy and subsequent lifestyle evolution as important elements of early fungal evolution. Taken together, this work provided a highly resolved genome-wide catalogue of gene family changes across fungal evolution. This suggests that the genome of pre-fungal ancestors may have been transformed into the archetypal fungal genome by a combination of gradual gene loss, turnover and two large duplication events rather than by abrupt changes, and consequently, that the taxonomically defined fungal kingdom does not represent a genomically uniform assemblage of extant species characterized by diagnostic synapomorphies.

evolutionary biology↗

The genome of Auriculariopsis ampla sheds light on fruiting body development and wood-decay of bark-inhabiting fungi

The Agaricomycetes are fruiting body forming fungi that produce some of the most efficient enzyme systems to degrade woody plant materials. Despite decades-long interest in the ecological and functional diversity of wood-decay types and in fruiting body development, the evolution of the genetic repertoires of both traits are incompletely known. Here, we sequenced and analyzed the genome of Auriculariopsis ampla, a close relative of the model species Schizophyllum commune. Comparative analyses of wood-decay genes in these and other 29 Agaricomycetes species revealed that the gene family composition of A. ampla and S. commune are transitional between that of white rot species and less efficient wood-degraders (brown rot, ectomycorrhizal). Rich repertoires of suberinase and tannase genes were found in both species, with tannases generally restricted to species that preferentially colonize bark-covered wood. Analyses of fruiting body transcriptomes in both A. ampla and S. commune highlighted a high rate of divergence of developmental gene expression. Several genes with conserved developmental expression were found, nevertheless, including 9 new transcription factors as well as small secreted proteins, some of which may serve as fruiting body-specific effector molecules. Taken together, the genome sequence and developmental transcriptome of Auriculariopsis ampla has highlighted novel aspects of wood-decay diversity and of fruiting body development in mushroom-forming fungi.

evolutionary biology↗

Comparative genomics reveals the origin of fungal hyphae and multicellularity

Hyphae represent a hallmark structure of multicellular fungi with immense importance in their life cycle, including foraging for nutrients, reproduction, or virulence. Hypha morphogenesis has been the subject to intense interest, yet, the origins and genetic underpinning of the evolution of hyphae are hardly known. Using comparative genomics, we here show that the emergence of hyphae correlates with multiple types of genetic changes, including alterations of gene structure, gene family diversification as well as co-option and exaptation of ancient eukaryotic genes (e.g. phagocytosis-related genes). Half of the gene families involved in hypha morphogenesis have homologs in unicellular fungi and non-fungal eukaryotes and show little or no duplications coincident with the origin of multicellular hyphae. Considerable gene family diversification was observed only in transcriptional regulators and genes related to cell wall synthesis and modification. Despite losing 35-46% of their genes, yeasts retained significantly more multicellularity-related genes than expected by chance. We identified 414 gene families that evolved in a correlated fashion with hyphal multicellularity and may have contributed to its evolution. Contrary to most multicellular lineages, the origin of hyphae did not correlate with the expansion of gene families encoding kinases, receptors or adhesive proteins. Our analyses suggest that fungi took a unique route to multicellularity that involved limited gene family diversification and extensive co-option of ancient eukaryotic genes.

evolutionary biology↗

Transcriptomic atlas of mushroom development highlights an independent origin of complex multicellularity

We constructed a reference atlas of mushroom formation based on developmental transcriptome data of six species and comparisons of >200 whole genomes, to elucidate the core genetic program of complex multicellularity and fruiting body development in mushroom-forming fungi (Agaricomycetes). Nearly 300 conserved gene families and >70 functional groups contained developmentally regulated genes from five to six species, covering functions related to fungal cell wall (FCW) remodeling, targeted protein degradation, signal transduction, adhesion and small secreted proteins (including effector-like orphan genes). Several of these families, including F-box proteins, protein kinases and cadherin-like proteins, showed massive expansions in Agaricomycetes, with many convergently expanded in multicellular plants and/or animals too, reflecting broad genetic convergence among independently evolved complex multicellular lineages. This study provides a novel entry point to studying mushroom development and complex multicellularity in one of the largest clades of complex eukaryotic organisms.

evolutionary biology↗

Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

Complex multicellularity comprises the most advanced level of organization evolved on Earth. It has evolved only a few times in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not seen in other lineages. In this article we review ecological, paleontological, developmental and genomic aspects of complex multicellularity in fungi and discuss the general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8-12 distinct fungal lineages, which show a patchy phylogenetic distribution, yet share some of the genetic mechanisms underlying complex multicellular development. To mechanistically explain the patchy distribution of complex multicellularity across the fungal tree of life we identify four key observations that need to be considered: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these; the universal conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain its pervasive occurrence in across the fungal tree of life.

evolutionary biology↗

Genome expansion and lineage-specific genetic innovations in the world’s largest organisms (Armillaria)

Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes using rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analyzed genomes of four Armillaria species and performed RNA-Seq and quantitative proteomic analysis on seven invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose degrading enzymes and lineage-specific genes likely involved in rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and shared cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.

evolutionary biology↗