Ethylene Regulates Differential Growth via BIG ARF-GEF-Dependent Post-Golgi Secretory Trafficking in Arabidopsis

Abstract

During early seedling development, the shoot apical meristem is protected from damage as the seedling emerges from soil by the formation of apical hook. Hook formation requires differential growth across the epidermis below the meristem in the hypocotyl. The plant hormones ethylene and auxin play key roles during apical hook development by controlling differential growth. We provide genetic and cell biological evidence for the role of ADP-ribosylation factor 1 (ARF1)-GTPase and its effector ARF-guanine-exchange factors (GEFs) of the Brefeldin A-inhibited GEF (BIG) family and GNOM in ethylene-and auxin-mediated control of hook development. We show that ARF-GEF GNOM acts early, whereas BIG ARF-GEFs act at a later stage of apical hook development. We show that the localization of ARF1 and BIG4 at the trans-Golgi network (TGN) depends on ECHIDNA (ECH), a plant homolog of yeast Triacylglycerol lipase (TLG2/SYP4) interacting protein Tgl2-Vesicle Protein 23 (TVP23). BIGs together with ECH and ARF1 mediate the secretion of AUX1 influx carrier to the plasma membrane from the TGN during hook development and defects in BIG or ARF1 result in insensitivity to ethylene. Thus, our data indicate a division of labor within the ARF-GEF family in mediating differential growth with GNOM acting during the formation phase whereas BIGs act during the hook maintenance phase downstream of plant hormone ethylene.

The Plant Trans-Golgi Network: Not Just a Matter of Distinction

“…Interestingly, and in contrast with GNOM, BIGs do not seem to affect recycling but only protein secretion (Richter et al, 2014). Such functional divergence could lie at the core of the observed stage-dependent, mutually exclusive involvement of GNOM and BIGs in the regulation of the secretion of AUX1 influx carrier to the plasma membrane from the TGN during hook development (Jonsson et al, 2017).…”

“…Two subclasses within the large A group of plant RABs, RABA2 and RABA3, identify a distinct TGN/EE membrane domain that functions in cargo delivery to the cell plate during cytokinesis (Chow et al, 2008). Whereas RABA2a defines TGN domains distinct from SYP61 vesicles, evidenced by differing lipid composition, RABA4b preferentially localizes to TGN SV sites together with SYP61, where it is involved in the transport of cell wall components (Preuss et al, 2004;Kang et al, 2011;Wattelet-Boyer et al, 2016;Jonsson et al, 2017). Another TGN domain harboring the secretory SNAREs VAMP721/722 and defined by RABA1 also has been suggested (Asaoka et al, 2013).…”

“…ECH also seems to be necessary for the proper TGN localization of the ADP-Ribosylation Factor1 (ARF1)-GTPase and the ARF-guanine-exchange factor BIG4. This pathway mediates secretion of the auxin carrier AUX1 from the TGN to the plasma membrane (PM) during hook development (Jonsson et al, 2017). In tobacco BY-2 cells, immunostaining of pectin showed that the Secretory Carrier Membrane Protein2 (SCAMP2) vesicles are involved in pectin transport (Toyooka et al, 2009).…”

On hormonal regulation of the dynamic apical hook development

“…The formation of an auxin gradient across hook curvature is mainly, but not exclusively, sustained by polar auxin transport (Beziat & Kleine‐Vehn, ). Spatial patterns of auxin transporters, and their regulation by subcellular events, in the apical hook have been extensively mapped with current prevailing cell biology experiments (Vandenbussche et al ., ; Zadnikova et al ., ; Willige et al ., ; Yu et al ., ; Beziat et al ., ; Jonsson et al ., ). However, how multiple transporters coordinately direct auxin flow during apical hook development is difficult to evaluate experimentally, and remains unclear.…”

Division of Labor during Apical Hook Formation

“…To tease apart the molecular mechanism underlying apical hook formation, Jonsson et al (2017) examined the contribution of ECH and ARF-GEFs to this process in Arabidopsis thaliana seedlings. Using a series of mutants and pharmacological treatments, they showed that the BIG1-4 ARF-GEFs act redundantly to maintain the apical hook once it has formed.…”