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How the Fungi got into shape : cellular organization and morphogenetic gene evolution in phylum Chytridiomycota reveals mechanisms underlying the evolution of fungal body diversity

University of British Columbia

With their threadlike hyphal cells, fungi can invade the surface of a cheese, secreting digestive enzymes and soaking up the spoils. Although most fungi feed with hyphae, phylum Chytridiomycota produces various alternative cell shapes. Here I address three hypotheses regarding the evolution of cell shape. Firstly, Fungi inherited core genes for cellular morphogenesis from their most recent common ancestor and diversification of these genes through evolutionary time potentially contributed to morphological novelty. My phylogenomic surveys revealed duplications in seven families of actin-binding proteins predating the radiation of fungal phyla. Synthesizing previous studies of the function, localization and evolutionary history of septin, myosin, and actin-binding proteins in yeasts and hyphal fungi enabled me to further hypothesize their roles during development in Chytridiomycota. Since Chytridiomycota diverged from moulds and mushrooms, each group evolved unique mechanisms for constructing different cell shapes using a shared ancestral molecular toolkit. Hyphal growth and septation require actin. My second hypothesis was that actin, a major cytoskeletal component, is also involved in morphogenesis in Chytridiomycota. Using fluorescence microscopy, I documented rhodamine phalloidin-stained actin cables, patches, sheets and perinuclear shells through development in Chytriomyces hyalinus. I disrupted the actin cytoskeleton with the chemical inhibitor latrunculin B. Observing actin patches concentrated at rhizoid tips and at cytoplasmic cleavage planes, and finding that actin integrity was essential for rhizoid proliferation in C. hyalinus both support a conserved role for actin in polarized growth and cytokinesis. Thirdly, I hypothesized that sustained tip growth and nuclear migration underlie the convergent evolution of hyphae and hypha-like growth forms. Chytriomyces hyalinus shows determinate growth that ceases once a zoosporangium matures. Phylogenies indicate that filamentous species in Chytridiomycota with indeterminate growth arose independently from ancestors with a determinate growth mode. I determined that actin organization and nuclear migration patterns in each species differed from one another and from hyphae, most likely as a result of their independent origins. In combination, phylogenetic analyses, molecular genetics, and microscopy are tearing away the curtains of time that mask the ever-changing molecular machinery that gave rise to an astounding diversity of form and function in modern fungi.

Text

2018-04-20

Attribution-NonCommercial-NoDerivatives 4.0 International

http://hdl.handle.net/2429/65536

Botany

University of British Columbia

UBCV

http://creativecommons.org/licenses/by-nc-nd/4.0/