Molecular and cellular dynamics of early embryonic cell divisions in Volvox carteri

Cell division is fundamental to all organisms and the green alga used here exhibits both key animal and plant functions. Specifically, we analyzed the molecular and cellular dynamics of early embryonic divisions of the multicellular green alga Volvox carteri (Chlamydomonadales). Relevant proteins related to mitosis and cytokinesis were identified in silico, the corresponding genes were cloned, fused to yfp, and stably expressed in Volvox, and the tagged proteins were studied by live-cell imaging. We reveal rearrangements of the microtubule cytoskeleton during centrosome separation, spindle formation, establishment of the phycoplast, and generation of previously unknown structures. The centrosomes participate in initiation of spindle formation and determination of spindle orientation. Although the nuclear envelope does not break down during early mitosis, intermixing of cytoplasm and nucleoplasm results in loss of nuclear identity. Finally, we present a model for mitosis in Volvox. Our study reveals enormous dynamics, clarifies spatio-temporal relationships of subcellular structures, and provides insight into the evolution of cell division.

Analysis of cell divisions of the microalga Volvox reveals enormous dynamics of cytoskeletal and membranous structures with coordination of intranuclear spindle formation by cytosolic centrosomes.

IN A NUTSHELLBackground: Mitosis, a type of cell division, is fundamental to all eukaryotic life and must be carried out very accurately. Even though the process of mitosis itself is highly conserved among eukaryotes, there are significant differences between animals, fungi, plants, and algae. From an evolutionary point of view, the green alga Volvox carteri used here possesses both key animal and plant functions and it exhibits important features of the last common eukaryotic ancestor that have been lost in other lineages. Prior to our work, a comprehensive in vivo analysis of the entire process of cell division in green algae was lacking.Question: How exactly does cell division work in green algae? How do the cytosolic centrosomes deal with the persistent nuclear envelope in this process? What is the relationship between different microtubular structures?Findings: Our study reveals enormous dynamics during mitosis, clarifies spatio-temporal relationships of subcellular structures, and provides insights into evolution of cell division. Although the nuclear envelope does not break down during early mitosis of Volvox, it becomes permeable and the nucleus temporarily loses its identity. Two microtubule-organizing centers, the centrosomes, located immediately outside the nuclear envelope participate in initiation of the mitotic spindle formation inside the nuclear envelope. This process also defines the orientation of the mitotic spindle. In cytokinesis, an algae-specific microtubule structure, the phycoplast, replaces the spindle. The microtubules of the phycoplast may play a direct role in promoting the cell membrane invagination of the cleavage furrow.Next steps: How are the massive rearrangements of subcellular structures regulated? What happens at the nuclear pores when the nuclear envelope becomes permeable at the onset of mitosis? What determines in later embryogenesis which cells then divide asymmetrically rather than symmetrically?