Unusual Roles of Secretory SNARE SYP132 in Plasma Membrane H⁺-ATPase Traffic and Vegetative Plant Growth

Abstract

The plasma membrane proton (H +)-ATPases of plants generate steep electrochemical gradients and activate osmotic solute uptake. H +-ATPase-mediated proton pumping orchestrates cellular homeostasis and is a prerequisite for plastic cell expansion and plant growth. All evidence suggests that the population of H +-ATPase proteins at the plasma membrane reflects a balance of their roles in exocytosis, endocytosis, and recycling. Auxin governs both traffic and activation of the plasma membrane H +-ATPase proteins already present at the membrane. As in other eukaryotes, in plants, SNARE-mediated membrane traffic influences the density of several proteins at the plasma membrane. Even so, H +-ATPase traffic, its relationship with SNAREs, and its regulation by auxin have remained enigmatic. Here, we identify the Arabidopsis (Arabidopsis thaliana) Qa-SNARE SYP132 (Syntaxin of Plants132) as a key factor in H +-ATPase traffic and demonstrate its association with endocytosis. SYP132 is a low-abundant, secretory SNARE that primarily localizes to the plasma membrane. We find that SYP132 expression is tightly regulated by auxin and that augmented SYP132 expression reduces the amount of H +-ATPase proteins at the plasma membrane. The physiological consequences of SYP132 overexpression include reduced apoplast acidification and suppressed vegetative growth. Thus, SYP132 plays unexpected and vital roles in auxin-regulated H +-ATPase traffic and associated functions at the plasma membrane.

Synergy among Exocyst and SNARE Interactions Identifies a Functional Hierarchy in Secretion during Vegetative Growth

“…Yet, the two Qa-SNARE null mutants show very different phenotypes in pathogen defense and abiotic stress resistance (Collins et al, 2003;Zhang et al, 2007;Eisenach et al, 2012) and the Qa-SNAREs mediate the traffic of different subsets of secretory cargo (Rehman et al, 2008;Waghmare et al, 2018). These, and associated studies (Reichardt et al, 2011;Hashimoto-Sugimoto et al, 2013;Xia et al, 2019;Zhang et al, 2019), implicate a functional network of trafficking and related regulatory protein partners that is substantially more dynamic than may be deduced from an analysis of gene families.…”

The SNARE SYP132 Fine-Tunes Proton Transporter Levels at the Plasma Membrane during Plant Growth

“…Together, the results presented by Xia et al (2019) clearly show that the Qa-SNARE SYP132 plays a role in intracellular trafficking of H + -ATPases and contributes to the regulation of auxin-mediated acid growth. The effects of SYP132 on H + -ATPase trafficking are somewhat counterintuitive, since SYP132 is a target SNARE localized to the PM.…”

“…SYP121 and SYP122 mediate the majority of PM trafficking and have some overlapping and distinct functions (Karnik et al, 2017). In this issue of Plant Physiology, Xia et al (2019) identify a role for the Qa-SNARE SYP132 in trafficking of H + -ATPases to the PM to facilitate acid growth.…”

SNARE Complexity in Arbuscular Mycorrhizal Symbiosis

“…This supports a sofar understudied role for PM-SNARE complex formation in the regulation of endocytic traffic in plants. Interestingly, it has recently been shown that AtSYP132 (the ortholog of MtSYP131) affects the endocytic traffic of an H+-ATPase, with which it interacts (Xia et al, 2019). Induced expression of AtSYP132 reduced the amount of H+-ATPase proteins at the PM thereby affecting the acidification of the cell wall.…”