Innovation and constraint leading to complex multicellularity in the Ascomycota

Abstract

The advent of complex multicellularity (CM) was a pivotal event in the evolution of animals, plants and fungi. In the fungal Ascomycota, CM is based on hyphal filaments and arose in the Pezizomycotina. The genus Neolecta defines an enigma: phylogenetically placed in a related group containing mostly yeasts, Neolecta nevertheless possesses Pezizomycotina-like CM. Here we sequence the Neolecta irregularis genome and identify CM-associated functions by searching for genes conserved in Neolecta and the Pezizomycotina, which are absent or divergent in budding or fission yeasts. This group of 1,050 genes is enriched for functions related to diverse endomembrane systems and their organization. Remarkably, most show evidence for divergence in both yeasts. Using functional genomics, we identify new genes involved in fungal complexification. Together, these data show that rudimentary multicellularity is deeply rooted in the Ascomycota. Extensive parallel gene divergence during simplification and constraint leading to CM suggest a deterministic process where shared modes of cellular organization select for similarly configured organelle- and transport-related machineries.

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

“…However, even among the Taphrinomycotina, which harbor mostly unicellular yeasts, species like Neolecta irregularis form ascocarps. Genome sequencing showed that Neolecta irregularis and Pezizomycotina share about 1,050 genes, not present in ascomycetous yeasts, with enriched functions related to complex multicellularity (334). Generally, five types of ascocarps are distinguished within the Pezizomycotina (apothecium, cleistothecium, gymnothecium, perithecium, or pseudothecium).…”

Fungal Genomes and Insights into the Evolution of the Kingdom

“…The data and approaches are only recently becoming available to support robust analyses to link genes to phenotypes. Some examples of successful applications of the approaches include the acquisition of enzymes needed for anaerobic growth by Saccharomyces [31–33], gains of subtilase genes related to animal associated lifestyles [34–36], genome reduction correlated to a yeast growth form [37,38], and changes in structure of centrioles for microtubule attachments [39]. …”

“…The free living yeasts in the Ascomycota and the Cryptomycota parasite Rozella typically have genomes in the 7- to 12-Mb range [80–84] and the Basidiomycota yeasts Cryptococcus are around 20 Mb [84–86]. Lineages containing yeast-forming species tend to have smaller genomes (such as Schizosaccharomyces and Ashyba ), but this apparent reduction has occurred independently and multiple times in fungal history [37,38,87]. …”

“…The filamentous Pezizomycotina filamentous fungi, sister to the Saccharomycetales yeasts, have genomes in the 35- to 45-Mb range and the Agaricomycotina fungi sister to the Pucciniomycotina are typically in the 45- to 60-Mb range. Analyses of gene gain and loss in yeast lineages have revealed that major gene losses occurred in the evolutionary history of these lineages indicating genome reduction in the transition to single-celled growth [37,38,87]. …”

Origin and evolution of the metazoan non-coding regulatory genome: Insights from the sponge Amphimedon queenslandica

“…Multicellular life has evolved independently at least 25 times, in groups as diverse as animals, fungi, plants, slime molds and seaweeds (Knoll, 2011;Nguyen et al, 2017;Niklas and Newman, 2013). All most complex living multicellular species, such as plants and animals, are descended from a single-celled ancestor, and understanding how these ancestors became multicellular remains a major challenge in the field of evolutionary biology.…”