Thinning and spreading: How the zebrafish embryo gets into shape

In teleost fish, the yolk syncytial layer is a multinucleate syncytium that functions as an extraembryonic signaling center to pattern embryonic tissues, coordinate morphogenesis and supply nutrients to the embryo. The external yolk syncytial nuclei (e-YSN) undergo microtubule dependent movements that distribute the nuclei over the large yolk mass. How e-YSN migration proceeds, and what role the elaborate longitudinal network of yolk microtubules plays is not understood but currently it is proposed that e-YSN are pulled downwards as the microtubule network shortens. Live imaging of yolk cell microtubules and nuclei reveal that the e-YSN do not appear to be pulled vegetally by microtubules but rather the nuclei move along a dynamic microtubule network. Our data are consistent with a cargo model in which the e-YSN move directly along microtubules by associating with microtubule motor proteins. We have also found that interfering with the function of either the plus-end directed microtubule motor kinesin-1, or the minus-end directed motor dynein significantly attenuated yolk nuclear movement. Based on the observation that the nuclei migrate without the centrosome, we propose that kinesin is the major motor involved, with dynein playing a role in navigating barriers to movement, as observed in other systems. In addition, blocking the outer nuclear membrane LINC complex protein Syne2a via KASH domain overexpression, also impaired e-YSN movement. Taken together, we propose that e-YSN movement is mediated by the LINC complex functioning as the adaptor between yolk nuclei and microtubule motor proteins. Our work provides new insights into the role of microtubules in morphogenesis of an extraembryonic tissue and further contributes to our broader understanding of nuclear migration mechanisms during development.