Evolutionary problems in centrosome and centriole biology

Abstract

Centrosomes have been an enigma to evolutionary biologists. Either they have been the subject of ill‐founded speculation or they have been ignored. Here, we highlight evolutionary paradoxes and problems of centrosome and centriole evolution and seek to understand them in the light of recent advances in centrosome biology. Most evolutionary accounts of centrosome evolution have been based on the hypothesis that centrosomes are replicators, independent of the nucleus and cytoplasm. It is now clear, however, that this hypothesis is not tenable. Instead, centrosomes are formed de novo each cell division, with the presence of an old centrosome regulating, but not essential for, the assembly of a new one. Centrosomes are the microtubule‐organizing centres of cells. They can potentially affect sensory and motor characters (as the basal body of cilia), as well as the movements of chromosomes during cell division. This latter role does not seem essential, however, except in male meiosis, and the reasons for this remain unclear. Although the centrosome is absent in some taxa, when it is present, its structure is extraordinarily conserved: in most taxa across eukaryotes, it does not appear to evolve at all. And yet a few insect groups display spectacular hypertrophy of the centrioles. We discuss how this might relate to the unusual reproductive system found in these insects. Finally, we discuss why the fate of centrosomes in sperm and early embryos might differ between different groups of animals.

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

“…The female gamete also eliminates or inactivates its centrioles to avoid multiple aster formation at fertilization and failed embryonic development [176][177][178]. Moreover, elimination of the maternal centrioles could eventually prevent spontaneous parthenogenetic development [179]. Therefore, the assembly of the zygotic centrosome at fertilization requires in most animals the direct involvement of the male gamete, which contributes not only its genetic material but also provides its centriole [45,176,180,181].…”

Loss and Rebirth of the Animal Microtubule Organizing Center: How Maternal Expression of Centrosomal Proteins Cooperates with the Sperm Centriole in Zygotic Centrosome Reformation

“…Centriole assembly thus generally uses pre‐existing structures to limit duplication in space and time. Such a coupling maintains a functional entity of the MTOC throughout interphase and limits replication to a single round . Although a whole variety of proteins are necessary for stable assembly and inheritance of centrioles, genetic, and biochemical experiments along with structural data in a variety of model systems have elucidated that centriole duplication requires a core module of components that at least include a master kinase, Plk4, or its orthologues and analogues, and the assembly regulators Ana2/Sas‐5/STIL and Sas‐6/SAS6 that are helped by the action of Sas‐4/CPAP and Spd‐2/CEP192 .…”

“…The mass of the PCM is drastically reduced and even proteins of the mother centriole itself may be replaced (“centriole reduction”). Varying from species to species, the contribution from the sperm ranges from bringing in two largely intact centrioles to supplying only one “reduced” centriole to fertilization . At least one centriole‐like structure, however, seems to be sufficient to generally trigger the assembly of a pair of MTOCs for the first mitotic chromosome segregation phase (Figure ).…”

“…Such a coupling maintains a functional entity of the MTOC throughout interphase and limits replication to a single round. [30] Although a whole variety of proteins are necessary for stable assembly and inheritance of centrioles, genetic, and biochemical experiments along with structural data in a variety of model systems have elucidated that centriole duplication requires a core module of components that at least include a master kinase, Plk4, or its orthologues and analogues, and the assembly regulators Ana2/Sas-5/STIL and Sas-6/SAS6 that are helped by the action of Sas-4/CPAP and Spd-2/ CEP192. [31] While Plk4 acts as a regulator to initially phosphorylate Sas-5/STIL, STIL programs Sas-6/SAS6 to directly shape the microtubule-based structure of daughter centrioles in nine-fold symmetry.…”

“…Varying from species to species, the contribution from the sperm ranges from bringing in two largely intact centrioles to supplying only one "reduced" centriole to fertilization. [30,58] At least one centriole-like structure, however, seems to be sufficient to generally trigger the assembly of a pair of MTOCs for the first mitotic chromosome segregation phase (Figure 3). Analysis of parthenogenesis in insects, on the other hand, indicates that the assembly of the first zygotic centrosome may occur without male contribution.…”