Delivery of endocytosed proteins to the cell–division plane requires change of pathway from recycling to secretion

Abstract

Membrane trafficking is essential to fundamental processes in eukaryotic life, including cell growth and division. In plant cytokinesis, post-Golgi trafficking mediates a massive flow of vesicles that form the partitioning membrane but its regulation remains poorly understood. Here, we identify functionally redundant Arabidopsis ARF guanine-nucleotide exchange factors (ARF-GEFs) BIG1–BIG4 as regulators of post-Golgi trafficking, mediating late secretion from the trans-Golgi network but not recycling of endocytosed proteins to the plasma membrane, although the TGN also functions as an early endosome in plants. In contrast, BIG1-4 are absolutely required for trafficking of both endocytosed and newly synthesized proteins to the cell–division plane during cytokinesis, counteracting recycling to the plasma membrane. This change from recycling to secretory trafficking pathway mediated by ARF-GEFs confers specificity of cargo delivery to the division plane and might thus ensure that the partitioning membrane is completed on time in the absence of a cytokinesis-interphase checkpoint.DOI: http://dx.doi.org/10.7554/eLife.02131.001

Vesicle Dynamics during Plant Cell Cytokinesis Reveals Distinct Developmental Phases

“…BIG3 is a BFA-resistant ARF-GEF protein involved in vesicle trafficking between the TGN and the cell plate in dividing cells (Richter et al, 2014). BFA treatment of wild-type plants does not affect the localization of KN at the cell plate but inhibits that of PEN1, a cycling plasma membrane syntaxin that normally accumulates at the cell plate in dividing cells.…”

“…Based on recent studies (Chow et al, 2008;Richter et al, 2014), it is reasonable to assume that recycled components converge into the late-secretory pathway at the TGN. 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.…”

“…(Dhonukshe et al, 2006;Reichardt et al, 2007;Chow et al, 2008;Lam et al, 2008;McMichael and Bednarek, 2013;Richter et al, 2014). It was shown that Golgiderived vesicles are the principal but not the only source contributing to the expanding cell plate, as other compartments composing the endocytic pathway seem to be involved as well (Reichardt et al, 2011;Richter et al, 2014). Since GFP-KN-labeled vesicles derive from the Golgi but not from late endosome or plasma membrane endocytosis, we used this marker here.…”

“…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).…”

Division of Labor during Apical Hook Formation

“…Members of the auxin influx carrier AUX/LIKE-AUX1 and efflux carrier PIN-FORMED (PIN) families, which direct polar auxin transport and thus influence the distribution of auxin, have been implicated in apical hook formation (Vandenbussche et al, 2010). Trans-Golgi network (TGN)-localized ECHIDNA (ECH) mediates the secretion of AUX1 during apical hook formation (Boutté et al, 2013), whereas members of the GNOM and BIG ADP-ribosylation factor-guanine exchange factor (ARF-GEFs) families function in the post-Golgi trafficking of PIN1, with the former mediating its polar recycling (Geldner et al, 2003) and the latter its secretion (Richter et al, 2014). Evidence suggests that a Brefeldin A (BFA)-resistant ARF-GEF also functions in AUX1 trafficking (KleineVehn et al, 2006).…”