Tracing the evolution of development among early diverging fungi

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Fungi can cause plant diseases, serve as mycorrhizal partners, and decompose litter and woody debris, all because of the tubular hyphae (filaments of cells, surrounded by a cell wall) that make up their bodies. Hyphae poke and penetrate into substrates while secreting digestive enzymes across their complex cell walls. The enzymes digest organic compounds into simple, diffusible molecules, which fungi absorb to fuel their growth, making fungi the most important terrestrial eukaryotic saprotrophs. The proposed research is directed towards understanding how fungi evolved and adapted to interdependence with land plants. New genome sequences are the key to unlocking secrets of the first steps in fungal evolution. Through our last round of Discovery Grant funding and a successful community sequencing collaboration with the US Joint Genome Institute (JGI), we sequenced and analyzed new genomes of 3 fungi that diverged from one another >600 million years ago, ~150 million years before the origin of vascular plants. We inferred that the ancestors of these fungi could digest the cell walls of algal relatives of land plants, being equipped with enzymes to breakdown the pectins that are a feature of plant walls. Our reconstructions of their form suggested that early fungi were microscopic in size and that they absorbed nutrients through a network of ‘rhizoids’ thin filaments of determinate growth that contain no nuclei. In our proposed research, we will sequence an additional 6-10 genomes, again in collaboration with JGI, analyzing them to find out how and when fungal secreted enzymes diversified, and how the proteins that control the fungal body shape changed as a microscopic rhizoidal ancestor evolved into a multicellular hyphal modern fungus. Specifically, we will: • Analyze evolution of the powerful cell wall degrading enzymes that fungi secrete as an adaptation to plant based nutrition. This research will reveal novel enzymes for cellulose decomposition with potential for industrial applications. • Trace the evolution of proteins such as septins and formins that control the points of growth and location of crosswalls in a cell, and result in characteristic fungal forms. Fungi and animals are close relatives in the big picture of eukaryote evolution, and our analysis of genes in ancestral fungi will suggest genes/proteins that may have guided polarity and the development of form in early animals. • Improve estimates of geological ages of fungi by developing evolutionary trees for modern fungi, and using corresponding fossils of known ages to date origins of fungal groups. Age estimates are widely used by the community of fungal molecular biologists as they strive to put patterns of gene and genome evolution into the perspective of geological time. This research will contribute to training 6 PhD, 3 MSc, and 6 BSc students to apply methods of cell and molecular biology to questions of fungal evolutionary biology.