Abstract
Cdc14 protein phosphatases are well known for regulating the eukaryotic cell cycle, particularly during mitosis. Here we reveal a distinctly new role for Cdc14 based on studies of the microbial eukaryote Phytophthora infestans, the Irish potato famine agent. While Cdc14 is transcribed constitutively in yeast and animal cells, the P. infestans ortholog is expressed exclusively in spore stages of the life cycle and not in vegetative hyphae where the bulk of mitosis takes place. PiCdc14 expression is first detected in nuclei at sporulation, and during zoospore formation the protein accumulates at the basal body, which is the site from which flagella develop. The association of PiCdc14 with basal bodies was supported by co-localization studies with the DIP13 basal body protein and flagellar β-tubulin, and by demonstrating the enrichment of PiCdc14 in purified flagella-basal body complexes. Overexpressing PiCdc14 did not cause defects in growth or mitosis in hyphae, but interfered with cytoplasmic partitioning during zoosporogenesis. This cytokinetic defect might relate to its ability to bind microtubules, which was shown using an in vitro cosedimentation assay. The use of gene silencing to reveal the precise function of PiCdc14 in flagella is not possible since we showed previously that silencing prevents the formation of the precursor stage, sporangia. Nevertheless, the association of Cdc14 with flagella and basal bodies is consistent with their phylogenetic distribution in eukaryotes, as species that lack the ability to produce flagella generally also lack Cdc14. An ancestral role of Cdc14 in the flagellar stage of eukaryotes is thereby proposed.
Highlights
Developmental processes are directed by regulatory proteins that coordinate cell division, cellular proliferation, and morphogenesis
Localization of PiCdc14 during P. infestans development N- and C-terminal fusions were constructed between PiCdc14 and green fluorescent protein (GFP) and named GFP/PiCdc14 and PiCdc14/GFP, respectively
The original discovery of Cdc14 as a regulator of mitosis in the S. cerevisiae cell cycle led scientists to search for similar roles in other fungi and in animals
Summary
Developmental processes are directed by regulatory proteins that coordinate cell division, cellular proliferation, and morphogenesis. One regulator with diverged functions is the dual-specificity protein phosphatase Cdc14 It is best known for its control of mitotic exit in Saccharomyces cerevisiae, which involves the antagonism of cyclin-dependent kinases and is regulated by the movement of Cdc into and out of the nucleolus during the cell cycle [4]. Even in S. cerevisiae, evidence is mounting for functions besides mitotic exit, such as in spindle stabilization and DNA replication [6] In metazoans such as Caenorhabditis elegans, humans, mouse, and Xenopus laevis, many roles in the cell cycle are described including in cytokinesis, G1/S and G2/M transitions, meiosis, and/or DNA damage checkpoints, especially in vertebrates which contain two or more Cdc genes [7,8,9,10,11]. Cdc of C. elegans helps program lineage-specific mitotic blocks during development [12] and a mouse Cdc regulates oocyte maturation [13]
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