Chromatin- and actin-mediated mitochondrial streaming leads to patterning of mitochondrial distribution in oocytes

Mitochondria are highly dynamic organelles, and their spatiotemporal organization is strictly regulated. While it has long been recognized that mitochondria in ovulated oocytes are concentrated in the spindle hemisphere, the mechanism remains unknown. Through live cell imaging and modeling, we have discovered that mitochondrial polarization in MII oocytes is achieved through two distinct mechanisms: (i) a mechanism in which mitochondria are transported by actin-driven cytoplasmic streaming that is delimited to the spindle hemisphere; (ii) an active, MYO19 dependent channeling mechanism that directs mitochondria from beneath the spindle to the polarized cortex bilaterally and perpendicular to the long axis of the MII spindle. This directionality in mitochondrial streaming patterns the ooplasm of the spindle hemisphere, creating mitochondria-rich and mitochondria-poor regions. These features explain the establishment of the polar gradient of mitochondria in MII oocytes and may provide new insight into the spatiotemporal organization of mitochondria in cells. In mature mouse eggs, mitochondria move from beneath the spindle to the cortex through a narrow corridor adjacent to chromosomes. This unexpected channeling role for chromosomes, with cytoplasmic flow, explains their asymmetric distribution.