Journal Article

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

Hasebe, Mitsuyasu, Van Damme, Daniël, Boruc, Joanna, Yamada, Moé, Kosetsu, Ken, Nishina, Momoko, Murata, Takashi, Goshima, Gohta

2017

Overview

Proper orientation of the cell division axis is critical for asymmetric cell divisions that underpin cell differentiation. In animals, centrosomes are the dominant microtubule organizing centers (MTOC) and play a pivotal role in axis determination by orienting the mitotic spindle. In land plants that lack centrosomes, a critical role of a microtubular ring structure, the preprophase band (PPB), has been observed in this process; the PPB is required for orienting (before prophase) and guiding (in telophase) the mitotic apparatus. However, plants must possess additional mechanisms to control the division axis, as certain cell types or mutants do not form PPBs. Here, using live imaging of the gametophore of the moss Physcomitrella patens, we identified acentrosomal MTOCs, which we termed “gametosomes,” appearing de novo and transiently in the prophase cytoplasm independent of PPB formation. We show that gametosomes are dispensable for spindle formation but required for metaphase spindle orientation. In some cells, gametosomes appeared reminiscent of the bipolar MT “polar cap” structure that forms transiently around the prophase nucleus in angiosperms. Specific disruption of the polar caps in tobacco cells misoriented the metaphase spindles and frequently altered the final division plane, indicating that they are functionally analogous to the gametosomes. These results suggest a broad use of transient MTOC structures as the spindle orientation machinery in plants, compensating for the evolutionary loss of centrosomes, to secure the initial orientation of the spindle in a spatial window that allows subsequent fine-tuning of the division plane axis by the guidance machinery.

• Publisher: National Academy of Sciences
• Subject: Actins - genetics / Actins - metabolism / Angiosperms / Asymmetric Cell Division / Biological Sciences / Bryopsida - cytology / Cell Biology / Cell differentiation / Cell division / Cells / Centrosomes / Cytoplasm / Cytoplasm - metabolism / Cytoplasm - ultrastructure / Machinery / Machinery and equipment / Metaphase / Microtubule-Associated Proteins - genetics / Microtubule-Associated Proteins - metabolism / Microtubules - metabolism / Nicotiana - cytology / Nicotiana - genetics / Nuclei / Nuclei (cytology) / Orientation / Plant Cells / Plant Proteins - genetics / Plant Proteins - metabolism / Plants, Genetically Modified / PNAS Plus / Polar caps / Prophase / Spindle Apparatus - metabolism / Spindles / Time-Lapse Imaging - methods / Tobacco / Tubulin - genetics / Tubulin - metabolism