Meiosis is a specialized cell division in sexually reproducing organisms before gamete formation. Following DNA replication, the canonical sequence in species with monocentric chromosomes is characterized by reductional segregation of homologous chromosomes during the first and equational segregation of sister chromatids during the second meiotic division. Species with holocentric chromosomes employ specific adaptations to ensure regular disjunction during meiosis. Here we present the analysis of two closely related plant species with holocentric chromosomes that display an inversion of the canonical meiotic sequence, with the equational division preceding the reductional. In-depth analysis of the meiotic divisions of Rhynchospora pubera and R. tenuis reveals that during meiosis I sister chromatids are bi-oriented, display amphitelic attachment to the spindle and are subsequently separated. During prophase II, chromatids are connected by thin chromatin threads that appear instrumental for the regular disjunction of homologous non-sister chromatids in meiosis II.
Highlights d A cascade of Aurora A/AIR-1, CEP192/SPD-2, and PLK-1 initiates PCM recruitment d SPD-2, PLK-1, and centrioles are required for mitotic PCM expansion d PLK-1 alone is required for PCM maintenance d Centrioles are required for centrosome structural integrity
The centriole is a conserved microtubule-based organelle essential for both centrosome formation and cilium biogenesis. Five conserved proteins for centriole duplication have been identified. Two of them, SAS-5 and SAS-6, physically interact with each other and are codependent for their targeting to procentrioles. However, it remains unclear how these two proteins interact at the molecular level. Here, we demonstrate that the short SAS-5 C-terminal domain (residues 390-404) specifically binds to a narrow central region (residues 275-288) of the SAS-6 coiled coil. This was supported by the crystal structure of the SAS-6 coiled-coil domain (CCD), which, together with mutagenesis studies, indicated that the association is mediated by synergistic hydrophobic and electrostatic interactions. The crystal structure also shows a periodic charge pattern along the SAS-6 CCD, which gives rise to an anti-parallel tetramer. Overall, our findings establish the molecular basis of the specific interaction between SAS-5 and SAS-6, and suggest that both proteins individually adopt an oligomeric conformation that is disrupted upon the formation of the hetero-complex to facilitate the correct assembly of the nine-fold symmetric centriole.
SummaryCentrosome function in cell division requires their duplication, once, and only once, per cell cycle. Underlying centrosome duplication are alternating cycles of centriole assembly and separation [1]. Work in vertebrates has implicated the cysteine protease separase in anaphase-coupled centriole separation (or disengagement) and identified this as a key step in licensing another round of assembly [2]. Current models have separase cleaving a physical link between centrioles, potentially cohesin [3, 4], that prevents reinitiation of centriole assembly unless disengaged. Here, we examine separase function in the C. elegans early embryo. We find that depletion impairs separation and consequently duplication of sperm-derived centrioles at the meiosis-mitosis transition. However, subsequent cycles proceed normally. Whereas mitotic centrioles separate in the context of cortical forces acting on a disassembling pericentriolar material, sperm centrioles are not associated with significant pericentriolar material or subject to strong forces. Increasing centrosomal microtubule nucleation restores sperm centriole separation and duplication in separase-depleted embryos, while forced pericentriolar material disassembly drives premature separation in mitosis. These results emphasize the critical role of cytoskeletal forces and the pericentriolar material in centriole separation. Separase contributes to separation where forces are limited, offering a potential explanation for results obtained in different experimental models [5–7].
SummaryCentrosomes are important regulators of microtubule organization in animal cells. Within the centrosome, microtubule nucleation and anchorage are mediated by proteins in the pericentriolar material (PCM) that accumulates around centrioles. The spatial organization of the PCM and the contribution of centrioles to its recruitment remain poorly understood. Previous work in the Drosophila embryo showed that the key PCM component Cnn specifically incorporates near centrioles, suggesting that centrioles play an ongoing role in PCM assembly [1]. It is currently unclear whether this model holds true in other organisms. Here, we examine PCM dynamics in the Caenorhabditis elegans embryo. We find that recruitment of the scaffold component SPD-5 occurs throughout the PCM. Incorporation of additional PCM subunits is therefore not limited to specific nucleation sites near centrioles, which has profound implications for the organization of the PCM lattice and the role of centrioles in centrosome assembly.
The centromere appears as a single constriction at mitotic metaphase in most eukaryotic chromosomes. Holokinetic chromosomes are the exception to this rule because they do not show any centromeric constrictions. Holokinetic chromosomes are usually forgotten in most reviews about centromeres, despite their presence in a number of animal and plant species. They are generally linked to very intriguing and unusual mechanisms of mitosis and meiosis. Holokinetic chromosomes differ from monocentric chromosomes not only in the extension of the kinetochore plate, but also in many other peculiar karyological features, which could be understood as the ‘holokinetic syndrome’ that is reviewed in detail. Together with holokinetic chromosomes we review neocentromeric activity, a similarly intriguing case of regions able to pull chromosomes towards the poles without showing the main components reported to be essential to centromeric function. A neocentromere is a chromosomal region different from the true centromere in structure, DNA sequence and location, but is able to lead chromosomes to the cell poles in special circumstances. Neocentromeres have been reported in plants and animals showing different features. Both in humans and Drosophila, neocentric activity appears in somatic cells with defective chromosomes lacking a functional centromere. In most cases in plants, neocentromeres appear in chromosomes which have normal centromeres, but are active only during meiosis. Because of examples such as spontaneous or induced neocentromeres and holokinetic chromosomes, it is becoming less surprising that different structures and DNA sequences of centromeres appear in evolution.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.