An evolutionary cell biology perspective into the diverging mechanisms of clathrin-mediated endocytosis in dikarya fungi
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Abstract
Clathrin-mediated endocytosis is an ancient eukaryotic trafficking pathway, which transports plasma membrane and associated cargo into the cell and is involved in numerous cell- and tissue-level processes. Cargo selection and clathrin-coated vesicle formation is mediated by over 60 proteins that assemble in a regular and sequential manner at the plasma membrane. Decades of endocytosis studies have followed the tenet that uncovering the conserved core molecular mechanisms is sufficient to understand a cellular process. However, this approach also revealed a number of cell type or species-related variations that challenge a universal conserved, core mechanism. In this paper, we refocus on the endocytic diversity to understand how evolution shapes endocytic mechanisms. We define a comparative evolutionary cell biology approach that uses dikarya fungi as a model clade and live-cell fluorescence microscopy to study endocytosis dynamics in three species: Saccharomyces cerevisiae , Schizosaccharomyces pombe and Ustilago maydis . Our results quantitatively define several phenotypic differences between the species. We uncover several differences that impact the endocytic early phase, the protein assembly order, actin regulation, membrane invagination and scission. These findings demonstrate a mosaic evolution of endocytic traits, suggest ancestral states and direction of changes. We also investigate the phenotypic plasticity and robustness against environmental conditions. Lastly, we demonstrate that relatively minor evolutionary changes can majorly impact endocytic phenotypes. These studies force an appreciation of endocytic variation as not auxiliary, but vital to mechanistic understanding of this conserved cellular pathway.
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Merging evolutionary and cell biology will be critical to uncover the evolutionary origins of cellular processes, link the molecular evolution to evolution of cellular phenotypes, and clarify the role of adaptation versus random genetic drift that drives cell level evolution [66].
This is a really beautiful work that answers a lot of important questions about the evolutionary diversity of an essential process, and leads to even more exciting question! Thank you for sharing this work!
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These data suggest that the membrane invagination length at the time of scission is different in each species: ∼100 nm in S. cerevisiae, ∼150 nm in S. pombe, and ∼50 nm in U. maydis.
Are there any physiological conditions that correlate with this finding?
Given the similar shape & size of U. maydis and S. pombe, I would have naively guessed that they'd have similar invagination lengths. Also, the short lifetime of endocytic proteins in U. maydis is consistent with shorter invaginations, but it looks like S. cerevisiae patch lifetimes are longer than S. pombe, but this doesn't correlate w/ invagination length.
Does the invagination depth scale with the turgor pressure? Or maybe the growth rate?
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All the proteins in the three species localized to small puncta at the plasma membrane consistent with a function in endocytosis (Figure 2A).
Beautiful images!
It looks like U. maydis consistently has a lot of cytoplasmic fluorescence, compared to the other yeasts.
Is their cytoplasm auto-fluorescent in untagged cells? If so, is it equally bright when grown in their preferred medium or could the synthetic medium be stressing them out?
or is it just a lot of tagged-protein that isn't localized to endocytic sites.
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All strains were cultured at 24°C unless otherwise specified
Was the growth rate of each species similar on the synthetic medium compared to the preferred medium?
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(SD)
Is this synthetic medium also supposed to be EMM? Table S2 does not have a recipe for SD medium but indicates S. cerevisiae grows on EMM.
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. However, lifetimes of the orthologs differed across species (Figure 3,
This is a beautiful visualization of the protein dynamics across species! It hammers home how the different modules of the machinery have such different effects across species! Breathtaking!
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S.cerevisiae
minor error: missing space
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