A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

Abstract

In teleost fish, the multinucleate yolk syncytial layer functions as an extraembryonic signaling center to pattern mesendoderm, coordinate morphogenesis and supply nutrients to the embryo. 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 the role of the yolk microtubules is not understood but it is proposed that e-YSN are pulled vegetally as the microtubule network shortens from the vegetal pole. Live imaging revealed that nuclei migrate along microtubules, consistent with a cargo model in which e-YSN are moved down the microtubules by direct association with motor proteins. We found that blocking the plus-end directed microtubule motor kinesin significantly attenuated yolk nuclear movement. Blocking the outer nuclear membrane LINC complex protein Syne2a, also slowed e-YSN movement. We propose that e-YSN movement is mediated by the LINC complex functioning as the adaptor between yolk nuclei and motor proteins. Our work provides new insights into the role of microtubules in morphogenesis of an extraembryonic tissue and further contributes to the understanding of nuclear migration mechanisms during development.