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Prasanna, A. N.

Publications and source records attributed to Prasanna, A. N..

4 recordsLinked to original sources

Unmatched level of molecular convergence among deeply divergent complex multicellular fungi

Convergent evolution is pervasive in nature, but it is poorly understood how various constraints and natural selection limit the diversity of evolvable phenotypes. Here, we report that, despite >650 million years of divergence, the same genes have repeatedly been co-opted for the development of complex multicellularity in the two largest clades of fungi--the Ascomycota and Basidiomycota. Co-opted genes have undergone duplications in both clades, resulting in >81% convergence across shared multicellularity-related families. This convergence is coupled with a rich repertoire of multicellularity-related genes in ancestors that predate complex multicellular fungi, suggesting that the coding capacity of early fungal genomes was well suited for the repeated evolution of complex multicellularity. Our work suggests that evolution may be predictable not only when organisms are closely related or are under similar selection pressures, but also if the genome biases the potential evolutionary trajectories organisms can take, even across large phylogenetic distances.

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↗

Multiple hidden processes complicate phylogenomic inference of deep Basidiomycota relationships

Resolving deep divergences in the fungal tree of life remains a challenging task even for analyses of genome-scale phylogenetic datasets. Relationships between Basidiomycota subphyla, the rusts (Pucciniomycotina), smuts (Ustilaginomycotina) and mushroom forming fungi (Agaricomycotina) represent a particularly challenging situation that posed problems to both traditional multigene and genome-scale phylogenetic studies. Here, we address basal Basidiomycota relationships using three different phylogenomic datasets, concatenated and gene tree-based analyses and examine the contribution of several potential sources of uncertainty, including fast-evolving sites, putative long-branch taxa, model violation and missing data. We inferred conflicting results with different datasets and under different models. Fast-evolving sites and oversimplified models of amino acid substitution favored the grouping of smuts with mushroom-forming fungi, often leading to maximal bootstrap support in both concatenation and Astral analyses. The most conserved datasets grouped rusts with mushroom forming fungi, although this relationship proved labile, sensitive to model choice, different data subsets and missing data. Excluding putative long branch taxa, genes with the highest proportions of missing data and/or genes with strong signal failed to reveal a consistent trend toward one or the other topology, suggesting that additional sources of conflict are at play too. Our analyses suggest that topologies uniting smuts with mushroom forming fungi can arise as a result of inappropriate modeling of amino acid sites that might be prone to systematic bias. While concatenated analyses yielded strong but conflicting support, individual gene trees mostly provided poor support for rusts, smuts and mushroom-forming fungi, suggesting that the true Basidiomycota tree might be in a part of the tree space that is difficult to access using both concatenation and gene tree based approaches. Thus, basal Basidiomycota relationships remain unresolved and might represent a phylogenetic problem that remains contentious even in the genomic era.

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↗