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Abstract
SAS-6 is required for centriole biogenesis in diverse eukaryotes. Here, we describe a novel family of SAS-6-like (SAS6L) proteins that share an N-terminal domain with SAS-6 but lack coiled-coil tails. SAS6L proteins are found in a subset of eukaryotes that contain SAS-6, including diverse protozoa and green algae. In the apicomplexan parasite Toxoplasma gondii, SAS-6 localizes to the centriole but SAS6L is found above the conoid, an enigmatic tubulin-containing structure found at the apex of a subset of alveolate organisms. Loss of SAS6L causes reduced fitness in Toxoplasma. The Trypanosoma brucei homolog of SAS6L localizes to the basal-plate region, the site in the axoneme where the central-pair microtubules are nucleated. When endogenous SAS6L is overexpressed in Toxoplasma tachyzoites or Trypanosoma trypomastigotes, it forms prominent filaments that extend through the cell cytoplasm, indicating that it retains a capacity to form higher-order structures despite lacking a coiled-coil domain. We conclude that although SAS6L proteins share a conserved domain with SAS-6, they are a functionally distinct family that predates the last common ancestor of eukaryotes. Moreover, the distinct localization of the SAS6L protein in Trypanosoma and Toxoplasma adds weight to the hypothesis that the conoid complex evolved from flagellar components.
Highlights
SAS-6 is required for centriole biogenesis in diverse eukaryotes
Each microtubule population is associated with a distinct microtubule-organizing centers (MTOCs); subpellicular microtubules radiate from the apical polar ring (APR), an MTOC unique to apicomplexan organisms [28, 30, 31], whereas spindle microtubules originate near a specialized region of the nuclear envelope termed the centrocone [32,33,34,35]
SAS6L-yellow fluorescent protein (YFP) filaments are insensitive to 1% Triton X-100 (TX-100), but 10 mg/ml DOC causes filament depolymerization apical SAS6L is retained. (D)
Summary
SAS-6 is required for centriole biogenesis in diverse eukaryotes. Here, we describe a novel family of SAS-6-like (SAS6L) proteins that share an N-terminal domain with SAS-6 but lack coiled-coil tails. In the apicomplexan parasite Toxoplasma gondii, SAS-6 localizes to the centriole but SAS6L is found above the conoid, an enigmatic tubulin-containing structure found at the apex of a subset of alveolate organisms. Centrioles and basal bodies are microtubule-based structures found in many eukaryotic lineages, including animals, lower plants, and diverse unicellular organisms [1,2,3]. Kinetoplastid parasites of the genera Trypanosoma and Leishmania cause human infectious diseases, including African sleeping sickness, Chagas disease, and kala azar [17] The shape of these organisms is maintained by an array of ϳ100 densely packed corset microtubules that underlie the plasma membrane [18]. Coccidian centrioles are composed of nine singlet microtubules and a central tubule and are organized in a parallel rather than an orthogonal configuration [27, 33, 40]
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