Abstract
Chromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functional diversification has occurred in various lineages. In order to better understand the evolution of genes involved in chromosome segregation in mammals, we analyzed some of the key components in the basal mammalian lineage of egg-laying mammals. The chromosome passenger complex is a multiprotein complex central to chromosome segregation during both mitosis and meiosis. It consists of survivin, borealin, inner centromere protein, and Aurora kinase B or C. We confirm the absence of Aurora kinase C in marsupials and show its absence in both platypus and echidna, which supports the current model of the evolution of Aurora kinases. High expression of AURKBC, an ancestor of AURKB and AURKC present in monotremes, suggests that this gene is performing all necessary meiotic functions in monotremes. Other genes of the chromosome passenger complex complex are present and conserved in monotremes, suggesting that their function has been preserved in mammals. Cohesins are another family of genes that are of vital importance for chromosome cohesion and segregation at mitosis and meiosis. Previous work has demonstrated an accumulation and differential loading of structural maintenance of chromosomes 3 (SMC3) on the platypus sex chromosome complex at meiotic prophase I. We investigated if a similar accumulation occurs in the echidna during meiosis I. In contrast to platypus, SMC3 was only found on the synaptonemal complex in echidna. This indicates that the specific distribution of SMC3 on the sex chromosome complex may have evolved specifically in platypus.
Highlights
The process of chromosome segregation involves a large number of components and requires tight regulation
Very little is known about segregation of complex chromosome multiples at meiosis and how these proteins might be involved in their segregation
Since very little is known about genes involved in chromosome segregation of monotremes, and given the phylogenetic position of monotremes and their extraordinary sex chromosome system, it is important to investigate the genes involved in segregation in this mammalian lineage
Summary
The process of chromosome segregation involves a large number of components and requires tight regulation. Very little is known about expression or functions of AURKs when it comes to meiosis—some studies have confirmed that, for instance, AURKA together with Polo-like kinase 1 (PLK1) is required for the correct migration of duplicated centrosomes at male meiosis I and II in order to form a bipolar spindle [8,9] It is unknown why there is the additional isoform AURKC present in germ cells of eutherian mammals, or why it is not present in marsupials. Apart from the study of Casey et al, there is practically no research investigating the segregation-related proteins in monotremes or more generally the segregation of chromosome multiples at meiosis Our analysis of these key components in the basal lineage of monotremes confir3mofe1d7 that AURKA and AURKBC are present, but AURKC is not, providing further clarification for the evolution of this gene family. This may be an indication that organization and segregation of the sex chromosome multiple is different between otherwise closely related species, raising potential implications for the cohesin involvement in the segregation of complex chromosome multiples
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