SNARE SYP132 mediates divergent trafficking of H+-ATPase AHA1 and antimicrobial PR1 during bacterial pathogenesis

Baena, G. , Xia, L. , Waghmare, S. and Karnik, R. (2022) SNARE SYP132 mediates divergent trafficking of H+-ATPase AHA1 and antimicrobial PR1 during bacterial pathogenesis. Plant Physiology, 189(3), pp. 1639-1661. (doi: 10.1093/plphys/kiac149) (PMID:35348763) (PMCID:PMC9237740)

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The vesicle trafficking SYNTAXIN OF PLANTS132 (SYP132) drives hormone-regulated endocytic traffic to suppress the density and function of plasma membrane (PM) H+-ATPases. In response to bacterial pathogens, it also promotes secretory traffic of antimicrobial pathogenesis-related (PR) proteins. These seemingly opposite actions of SYP132 raise questions about the mechanistic connections between the two, likely independent, membrane trafficking pathways intersecting plant growth and immunity. To study SYP132 and associated trafficking of PM H+-ATPase 1 (AHA1) and PATHOGENESIS-RELATED PROTEIN1 (PR1) during pathogenesis, we used the virulent Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) bacteria for infection of Arabidopsis (Arabidopsis thaliana) plants. SYP132 overexpression suppressed bacterial infection in plants through the stomatal route. However, bacterial infection was enhanced when bacteria were infiltrated into leaf tissue to bypass stomatal defenses. Tracking time-dependent changes in native AHA1 and SYP132 abundance, cellular distribution, and function, we discovered that bacterial pathogen infection triggers AHA1 and SYP132 internalization from the plasma membrane. AHA1 bound to SYP132 through its regulatory SNARE Habc domain, and these interactions affected PM H+-ATPase traffic. Remarkably, using the Arabidopsis aha1 mutant, we discovered that AHA1 is essential for moderating SYP132 abundance and associated secretion of PR1 at the plasma membrane for pathogen defense. Thus, we show that during pathogenesis SYP132 coordinates AHA1 with opposing effects on the traffic of AHA1 and PR1.

Item Type:Articles
Additional Information:This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) grants (BB/S017348/1, BB/S506734/1) the Royal Society grant (RG160493) and Royal Society University Research Fellowship awards (UF150364, URF\R\211002), the Wellcome trust (204820/Z/16/Z) and Leadership funding (University of Glasgow) to R.K. L.X. was funded by China Scholarship Council PhD studentship (201706300012).
Glasgow Author(s) Enlighten ID:Baena, Dr Guillermo and Karnik, Dr Rucha and Xia, Mr Lingfeng and Waghmare, Dr Sakharam
Authors: Baena, G., Xia, L., Waghmare, S., and Karnik, R.
College/School:College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
Journal Name:Plant Physiology
Publisher:Oxford University Press
ISSN (Online):1532-2548
Published Online:28 March 2022
Copyright Holders:Copyright © 2022 The Authors
First Published:First published in Plant Physiology 189(3): 1639-1661
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
305007SNARE endocytosis and secretory vesicle reuse in plant growth-defense trade offsRucha KarnikBiotechnology and Biological Sciences Research Council (BBSRC)BB/S017348/1Institute of Molecular, Cell & Systems Biology
302389BBSRC IAA applicationGraeme MilliganBiotechnology and Biological Sciences Research Council (BBSRC)BB/S506734/1Institute of Molecular, Cell & Systems Biology
173990Proton Transport Modulators - Spatial Regulation and Effects on Plant PhysiologyRucha KarnikThe Royal Society (ROYSOC)RG160493MCSB - Plant Sciences
173284Hormone-Regulated Membrane Traffic and Plant MorphogenesisRucha KarnikThe Royal Society (ROYSOC)UF150364MCSB - Plant Sciences
173707Institutional Strategic Support Fund (2016)Anna DominiczakWellcome Trust (WELLCOTR)204820/Z/16/ZInstitute of Cardiovascular & Medical Sciences