K+ channel and SEC11 binding exchange regulates SNARE assembly for secretory traffic

Waghmare, S., Lefoulon, C., Zhang, B. , Lileikyte, E., Donald, N. and Blatt, M. (2019) K+ channel and SEC11 binding exchange regulates SNARE assembly for secretory traffic. Plant Physiology, 181, pp. 1096-1113. (doi: 10.1104/pp.19.00919) (PMID:31548266)

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Abstract

Cell expansion requires that ion transport and secretory membrane traffic operate in concert. Evidence from Arabidopsis (Arabidopsis thaliana) indicates that such coordination is mediated by physical interactions between subsets of so-called SNARE proteins, which drive the final stages of vesicle fusion, and K+ channels that facilitate uptake of the cation to maintain cell turgor pressure as the cell expands. However, the sequence of SNARE binding with the K+ channels and its interweaving within the events of SNARE complex assembly for exocytosis has remained unclear. We have combined protein-protein interaction and electrophysiological analyses to resolve the binding interactions of the hetero-oligomeric associations. We find that the RYxxWE motif, located within the voltage sensor of the K+ channels, is a nexus for multiple SNARE interactions. Of these, K+ channel binding and its displacement of the regulatory protein SEC11 is critical to prime the Qa-SNARE SYP121. Our results indicate a stabilizing role for the Qbc-SNARE SNAP33 in Qa-SNARE transition to SNARE complex assembly with the R-SNARE VAMP721. They also suggest that, on its own, the R-SNARE enters an anomalous binding mode with the channels, possibly as a fail-safe to ensure a correct binding sequence. Thus, we suggest that SYP121 binding to the K+ channels serves the role of a primary trigger to initiate assembly of the secretory machinery for exocytosis.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Blatt, Professor Michael and Zhang, Dr Ben and Waghmare, Dr Sakharam and Lileikyte, Miss Edita and Donald, Miss Naomi and Lefoulon, Dr Cecile
Authors: Waghmare, S., Lefoulon, C., Zhang, B., Lileikyte, E., Donald, N., and Blatt, M.
College/School: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:23 September 2019
Copyright Holders:Copyright © 2019 American Society of Plant Biologists
First Published:First published in Plant Physiology 2019 181:1096-1113
Publisher Policy:Reproduced under a Creative Commons license

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
703441Dissecting a new and vital checkpoint in SNARE recycling and plant growthMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/N006909/1RI MOLECULAR CELL & SYSTEMS BIOLOGY
656891Analysing GORK clustering for enhanced stomatal controlMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/M001601/1RI MOLECULAR CELL & SYSTEMS BIOLOGY
172632NEURICEMichael BlattEuropean Commission (EC)678168MCSB - Plant Sciences