Self-Organization of Dynein Motors Generates Meiotic Nuclear Oscillations

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Abstract
Meiotic nuclear oscillations in the fission yeast Schizosaccharomyces pombe are crucial for proper chromosome pairing and recombination. We report a mechanism of these oscillations on the basis of collective behavior of dynein motors linking the cell cortex and dynamic microtubules that extend from the spindle pole body in opposite directions. By combining quantitative live cell imaging and laser ablation with a theoretical description, we show that dynein dynamically redistributes in the cell in response to load forces, resulting in more dynein attached to the leading than to the trailing microtubules. The redistribution of motors introduces an asymmetry of motor forces pulling in opposite directions, leading to the generation of oscillations. Our work provides the first direct in vivo observation of self-organized dynamic dynein distributions, which, owing to the intrinsic motor properties, generate regular large-scale movements in the cell. A key aspect of life is sexual reproduction, which involves the mixing of genetic material during meiosis. In fission yeast and other organisms, the successful mixing and recombining of the chromosomes requires concerted movement of the nucleus. This phenomenon is driven by molecular motors that move the nucleus back and forth inside the cell with the aid of microtubules. How motors and microtubules work together to produce these large-scale movements, however, remains a mystery. Here, we show that nuclear oscillation in fission yeast occurs as motor proteins redistribute from microtubules behind the moving nucleus to those in front of the nucleus, generating an asymmetric distribution of motors and, consequently, of pulling force. By combining quantitative live cell imaging and laser ablation with a theoretical model, we find that this dynamic motor redistribution occurs purely as a result of changes in the mechanical strain sensed by the motor proteins. This work therefore demonstrates that spatio-temporal pattern formation within a cell can occur as a result of self-organization driven by mechanical cues, rather than via the more commonly observed mechanisms of conventional molecular signaling or self-organization driven by biochemical reactions and diffusion.