Centrioles and kinetosomes: form, function, and evolution.

Abstract

We review the literature on centrioles, kinetosomes, and other microtubule organizing centers (MTOCs) in animal, plant, and protist cells in the context of the Henneguy-Lenhossék theory of 1899. This 100-year-old cytological theory, valid today, defines centrioles and kinetosomes as identical, homologous but developmentally distinguishable structures. Centrioles (paired constituents of mitotic centrosomes in animal cells) become kinetosomes (ciliary basal bodies) when their 9(2) + 2 microtubular axonemes grow outward. During mitosis in Chlamydomonas, the kinetosomes are segregated at the poles of the mitotic spindle. Mitotic centrioles function as organelles of motility in many protists, though nowhere is this centriole-kinetosome relation more clearly seen than in the karyomastigont structure (kinetosome-nucleus-Golgi complex organellar system) of the trichomonads and other amitochondriate parabasalids. Constituent sequences of mitotic spindle-centriole-kinetosome proteins (gamma-tubulin, pericentrin, and the cyclin-dependent kinases Cdc2 and Cdc3, members of the centrin family) are conserved across taxa, occurring in animal and protist centrioles, plant MTOCs, and fungal spindle pole bodies. We review ultrastructural and molecular data on these and other important MTOC proteins, and present a model whereby the cytological arrangement of centrioles (i.e., orthogonal pairs as in centrosomes) may have originated. We compare and contrast endogenous and exogenous (bacterial symbiont integration) models for the evolution of centriole-kinetosomes (c-ks), with illustrative examples from Kingdom Protoctista.