Unusual roles of secretory SNARE SYP132 in plasma membrane H+-ATPase traffic and vegetative plant growth

Xia, L., Marques-Bueno, M. M., Bruce, C. G. and Karnik, R. (2019) Unusual roles of secretory SNARE SYP132 in plasma membrane H+-ATPase traffic and vegetative plant growth. Plant Physiology, 180(2), pp. 837-858. (doi: 10.1104/pp.19.00266) (PMID:30926657)

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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 (soluble N-ethylmaleimide-sensitive factor attachment protein receptor)-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 Plants 132) 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 over-expression 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.

Item Type:Articles
Additional Information:This work was supported by the Royal Society University Research Fellowship UF150364 and Royal Society research grant RG160493 to RK. LX is funded by a PhD scholarship from the China Scholarship Council. CB and MMB were supported by the University of Glasgow Leadership funds to RK
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Marques-Bueno, Dr Maria Del Mar and Karnik, Dr Rucha and Bruce, Mr Craig and Xia, Lingfeng
Authors: Xia, L., Marques-Bueno, M. M., Bruce, C. G., and Karnik, R.
College/School:College of Medical Veterinary and Life Sciences
College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Plant Physiology
Publisher:American Society of Plant Biologists
ISSN:0032-0889
ISSN (Online):1532-2548
Published Online:29 March 2019
Copyright Holders:Copyright © 2019 The American Society of Plant Biologists
First Published:First published in Plant Physiology 180(2):837-858
Publisher Policy:Reproduced in accordance with the copyright policy of the publisher

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
714451Hormone-Regulated Membrane Traffic and Plant MorphogenesisRucha KarnikThe Royal Society (ROYSOC)UF150364RI MOLECULAR CELL & SYSTEMS BIOLOGY
755891Proton Transport Modulators - Spatial Regulation and Effects on Plant PhysiologyRucha KarnikThe Royal Society (ROYSOC)RG160493RI MOLECULAR CELL & SYSTEMS BIOLOGY