Plant Cytokinesis Is Orchestrated by the Sequential Action of the TRAPPII and Exocyst Tethering Complexes

Abstract

Plant cytokinesis is initiated in a transient membrane compartment, the cell plate, and completed by a process of maturation during which the cell plate becomes a cross wall. How the transition from juvenile to adult stages occurs is poorly understood. In this study, we monitor the Arabidopsis transport protein particle II (TRAPPII) and exocyst tethering complexes throughout cytokinesis. We show that their appearance is predominantly sequential, with brief overlap at the onset and end of cytokinesis. The TRAPPII complex is required for cell plate biogenesis, and the exocyst is required for cell plate maturation. The TRAPPII complex sorts plasma membrane proteins, including exocyst subunits, at the cell plate throughout cytokinesis. We show that the two tethering complexes physically interact and propose that their coordinated action may orchestrate not only plant but also animal cytokinesis.

Vesicle Dynamics during Plant Cell Cytokinesis Reveals Distinct Developmental Phases

“…This means that, during IPA, the components forming the cell plate will have a mosaic origin and can derive from both the ER and the Golgi that localize in the vicinity of the future cell plate (Nebenführ et al, 2000;Rybak et al, 2014) as well as from the outer envelope of the cell (plasma membrane and parental cell wall), although the respective contribution of one source may dwarf the other.…”

“…While the resolution of optical micrographs does not allow identifying the anatomy of the cell plate at this stage, electron microscopy-based studies suggest that, during the PCG, corresponding to the solid phragmoplast stage, the dumbbell-shaped intermediates fuse to form the tubulovesicular network (Seguí-Simarro et al, 2004, 2008. Rybak et al (2014) recently proposed that TRAPPII is the main tethering complex that drives the fusion of the TGN-derived vesicles to build the expanding cell plate. The biogenesis stage undoubtedly correlates with the intense vesicle traffic that we observe during IPA and PCG, as indicated by both the rapid and nearly complete recovery of cell plate fluorescence after photobleaching and the extremely rough cell plate surface observed in four-dimensional (4D) reconstruction series.…”

“…The initiation of the formation of the cell plate corresponds to the fusion of vesicles in the CPAM enriched in exocyst-tethering complexes (including EXO70A1 and EXO84b; Fendrych et al, 2010;Rybak et al, 2014). It is intriguing that the exocyst complexes move back and forth between the plasma membrane and the cytoplasm (Fendrych et al, 2010(Fendrych et al, , 2013.…”

“…Evidence for a Golgi-based origin of vesicles stems from the presence of methylesterified pectins (as deduced from JIM7 label; Rybak et al, 2014) in the early stage of the cell plate. Furthermore, during this early stage, cell plate formation is prevented when ER-toGolgi transport is inhibited by low BFA concentration (Ritzenthaler et al, 2002;Lam et al, 2009;Langhans et al, 2011) or when CHX is administered prior to DNA condensation to interfere with de novo protein synthesis.…”

“…The trans-Golgi network (TGN) is considered the cornerstone compartment through which either newly synthesized Golgi-derived proteins and polysaccharides, or endocytosed material (proteins, polysaccharides, and lipids) from the plasma membrane and cell wall, and potentially from late endosomes, build the new cell plate (Chow et al, 2008;Thellmann et al, 2010;Richter et al, 2014;Rybak et al, 2014). 3D electron tomography has yielded exquisite ultrastructural details about the anatomy of the growing cell plate and the fusion of vesicles between each other and to the plate (Samuels et al, 1995;Austin et al, 2005).…”