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The Role and Mechanism of Meiotic Chromosome Motion in C. elegans

Abstract

Proper meiotic chromosome segregation in C. elegans requires homolog pairing, synapsis, and recombination. The mechanisms underlying homologous chromosome pairing remain poorly understood. In C. elegans, as in many other eukaryotes, pairing is accompanied by a global rearrangement of chromosomes. Work from the Dernburg lab and others has found that this rearrangement is driven through the association of special chromosome regions known as Pairing Centers (PCs) with nuclear envelope proteins and cytoskeletal components (Phillips et al. 2005, Sato et al. 2009). Using fluorescent markers for nuclear envelope attachment sites and Pairing Centers, I analyzed prophase chromosome dynamics through real-time imaging and quantitative motion tracking. My results reveal a dramatic increase in chromosome motion at the onset of chromosome pairing that persists after homologous loci are paired. I show that this increased mobility correlates with the formation of NE patches, and that the increase in motion that accompanies meiotic entry is abrogated by knockdown of cytoplasmic dynein. These rapid motions are also sensitive to depolymerization of microtubules by colchicine, but are not affected by treatment with Latrunculin A. In addition, fluorescent labeling of whole chromosomes suggests that meiotic chromosome motion is driven primarily by the PC end of chromosomes and that the chromosome is quite flexible. These data support a model in which meiotic chromosome motion is promoted by a small number of fast, microtubule-dependent, motor-driven movements that augment the smaller, likely diffusive motions seen prior to meiosis. The observation that fast motions persist well after pairing is completed suggests additional roles in chromosome synapsis or recombination, and are consistent with the idea that rapid motions function to destabilize inappropriate, non-homologous interactions.

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