Spatial constraints on chromosomes are instrumental to meiotic pairing

Abstract

In 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 (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. Lack of sequence similarity between the Tetrahymena genes 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. We therefore speculate that centromere clustering may have been the primordial mechanism for chromosome pairing in early eukaryotes.