Abstract
ABSTRACTIn most eukaryotes, the meiotic chromosomal bouquet (comprising clustered chromosome ends) provides an ordered chromosome arrangement that facilitates pairing and recombination between homologous chromosomes. In the protist Tetrahymena thermophila, the meiotic prophase nucleus stretches enormously, and chromosomes assume a bouquet-like arrangement in which telomeres and centromeres are attached to opposite poles of the nucleus. We have identified and characterized three meiosis-specific genes [meiotic nuclear elongation 1-3 (MELG1-3)] that control nuclear elongation, and centromere and telomere clustering. The Melg proteins interact with cytoskeletal and telomere-associated proteins, and probably repurpose them for reorganizing the meiotic prophase nucleus. A lack of sequence similarity between the Tetrahymena proteins responsible for telomere clustering and bouquet proteins of other organisms suggests that the Tetrahymena bouquet is analogous, rather than homologous, to the conserved eukaryotic bouquet. We also report that centromere clustering is more important than telomere clustering for homologous pairing. Therefore, we speculate that centromere clustering may have been the primordial mechanism for chromosome pairing in early eukaryotes.
Highlights
The issue of how homologous chromosomes move and find each other during meiotic prophase is much debated
Among the over 80 candidate meiosis genes that were knocked out, we identified three genes that are essential for the full elongation of prophase nuclei (Fig. 2A-C; Fig. S1)
Nuclear elongation promotes pairing T. thermophila micronuclei undergo a striking reorganization during meiosis (Fig. 1) – they elongate considerably, and chromosome centromeres and telomeres migrate to opposite tips of the nucleus
Summary
The issue of how homologous chromosomes move and find each other during meiotic prophase is much debated. Centromeres or other specialized chromosome regions, together with movements driven by cytoskeletal elements, enables chromosomes to find and pair with their homologous partners. The bouquet arrangement with telomeres clustered at the nuclear periphery is prevalent in most eukaryotes (Scherthan, 2001; Zickler and Kleckner, 2016), additional or alternative mechanisms for aligning chromosomes do exist (see Da Ines and White, 2015; Loidl, 2016). Meiotic prophase nuclei of the unicellular protist Tetrahymena thermophila undergo a remarkable reorganization – they stretch to approximately twice the length of the cell (Sugai and Hiwatashi, 1974; Fig. 1).
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