Concerted Action of Evolutionarily Ancient and Novel SNARE Complexes in Flowering-Plant Cytokinesis

Membrane vesicles delivered to the cell-division plane fuse with one another to form the partitioning membrane during plant cytokinesis, starting in the cell center. In Arabidopsis, this requires SNARE complexes involving the cytokinesis-specific Qa-SNARE KNOLLE. However, cytokinesis still occurs in knolle mutant embryos, suggesting contributions from KNOLLE-independent SNARE complexes. Here we show that Qa-SNARE SYP132, having counterparts in lower plants, functionally overlaps with the flowering plant-specific KNOLLE. SYP132 mutation causes cytokinesis defects, knolle syp132 double mutants consist of only one or a few multi-nucleate cells, and SYP132 has the same SNARE partners as KNOLLE. SYP132 and KNOLLE also have non-overlapping functions in secretion and in cellularization of the embryo-nourishing endosperm resulting from double fertilization unique to flowering plants. Evolutionarily ancient non-specialized SNARE complexes originating in algae were thus amended by the appearance of cytokinesis-specific SNARE complexes, meeting the high demand for membrane-fusion capacity during endosperm cellularization in angiosperms. •Qa-SNAREs SYP132 and KNOLLE function in cytokinesis in Arabidopsis•SYP132 also functions in the secretory pathway, unlike KNOLLE•KNOLLE is an evolutionarily derived Qa-SNARE specializing in angiosperm cytokinesis•SYP132 is a non-specialized ancient Qa-SNARE originating in alga-like ancestors In plant cytokinesis, SNARE complexes mediate vesicle fusion for partitioning membrane formation. Park et al. show that evolutionarily ancient Qa-SNARE SYP132 functionally overlaps with flowering plant- and cytokinesis-specific Qa-SNARE KNOLLE. KNOLLE acquisition may have been due to high demand for membrane-fusion capacity during endosperm cellularization in flowering plants.