Abstract
Proteins of the FGR1 oncogene partner (or FOP) family are found at microtubule organizing centres (MTOCs) including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing (in contrast with mammalian cells, where FOP is essential for flagellum assembly) depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising because PFR nucleation commences approximately 2 µm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localization of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.
Highlights
Coupled, N-terminally located TOF-LisH motifs define a small family of eukaryotic proteins—the FOP family—members of which are required for ciliogenesis in flagellate eukaryotes, and cortical cytoskeleton organization in plant cells
We report here the conservation of OFD1 and FOP-like proteins in trypanosomatid protists, and our unexpected observation that a T. brucei FOP-like protein is essential for assembly of the extra-axonemal paraflagellar rod (PFR), but not the axoneme itself
The predicted proteins encoded by Tb927.5.4090 and Tb927.10.3000 are not immediately recognizable as orthologous to any particular FOP family protein
Summary
N-terminally located TOF-LisH motifs define a small family of eukaryotic proteins—the FOP family—members of which are required for ciliogenesis in flagellate eukaryotes, and cortical cytoskeleton organization in plant cells. In animal cells, OFD1, FOR20 and FOP are all found at the base of cilia associated with basal bodies (or centrioles), either at the level of the triplet microtubule barrel or the transition zone. The microtubule axoneme (the defining structure of all eukaryotic flagella or cilia) extends from the basal body; the transition zone defines the most proximal region of the flagellum and exhibits its own particular architecture, where Y-shaped projections link axoneme outer-doublet microtubules to the flagellar membrane [9].
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