Arabidopsis SNARE SYP132 impacts on PIP2;1 trafficking and function in salinity stress

Baena, G. , Xia, L. , Waghmare, S. , Yu, Z., Guo, Y., Blatt, M. R. , Zhang, B. and Karnik, R. (2024) Arabidopsis SNARE SYP132 impacts on PIP2;1 trafficking and function in salinity stress. Plant Journal, (doi: 10.1111/tpj.16649) (PMID:38289468) (Early Online Publication)

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Abstract

In plants so-called plasma membrane intrinsic proteins (PIPs) are major water channels governing plant water status. Membrane trafficking contributes to functional regulation of major PIPs and is crucial for abiotic stress resilience. Arabidopsis PIP2;1 is rapidly internalised from the plasma membrane in response to high salinity to regulate osmotic water transport, but knowledge of the underlying mechanisms is fragmentary. Here we show that PIP2;1 occurs in complex with SYNTAXIN OF PLANTS 132 (SYP132) together with the plasma membrane H+-ATPase AHA1 as evidenced through in vivo and in vitro analysis. SYP132 is a multifaceted vesicle trafficking protein, known to interact with AHA1 and promote endocytosis to impact growth and pathogen defence. Tracking native proteins in immunoblot analysis, we found that salinity stress enhances SYP132 interactions with PIP2;1 and PIP2;2 isoforms to promote redistribution of the water channels away from the plasma membrane. Concurrently, AHA1 binding within the SYP132-complex was significantly reduced under salinity stress and increased the density of AHA1 proteins at the plasma membrane in leaf tissue. Manipulating SYP132 function in Arabidopsis thaliana enhanced resilience to salinity stress and analysis in heterologous systems suggested that the SNARE influences PIP2;1 osmotic water permeability. We propose therefore that SYP132 coordinates AHA1 and PIP2;1 abundance at the plasma membrane and influences leaf hydraulics to regulate plant responses to abiotic stress signals.

Item Type:Articles
Additional Information:This work was supported by grants from the Biotechnology and Biological Sciences Research Council (BB/S017348/1, BB/S506734/1, BB/X013383/1), Royal Society (RG160493), Royal Society University Research Fellowship (UF150364, URF\R\211002) to RK and Wellcome ISSF Excellence and Innovation Catalyst Funding (204820/Z/16/Z), BBSRC Agriculture, Health and Food funding (BB/W510658/1) to GB, and funding to BZ from the National Natural Science Foundation of China (No. 32000210, 32272012), and Research Project Support by Shanxi Scholarship Council of China (No.2021-015), and Funding Program for the Scientific Activities of Selected Returned Overseas Professionals in Shanxi Province (No. 20230003). China Scholarship Council PhD studentship funding supports LX (201706300012) and ZY (202006350012).
Keywords:Membrane traffic, SNARE, aquaporin, stomata, transport, Arabidopsis thaliana.
Status:Early Online Publication
Refereed:Yes
Glasgow Author(s) Enlighten ID:Yu, Ms ZhiYi and Baena, Dr Guillermo and Karnik, Dr Rucha and Blatt, Professor Michael and Zhang, Dr Ben and Xia, Mr Lingfeng and Waghmare, Dr Sakharam
Authors: Baena, G., Xia, L., Waghmare, S., Yu, Z., Guo, Y., Blatt, M. R., Zhang, B., and Karnik, R.
College/School:College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
Journal Name:Plant Journal
Publisher:Wiley
ISSN:0960-7412
ISSN (Online):1365-313X
Published Online:30 January 2024
Copyright Holders:Copyright © 2024 The Authors
First Published:First published in Plant Journal 2024
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/S017348/1School of Molecular Biosciences
302389BBSRC IAA applicationGraeme MilliganBiotechnology and Biological Sciences Research Council (BBSRC)BB/S506734/1School of Molecular Biosciences
319189A SNARE-Aquaporin complex in stomatal hydraulicsMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/X013383/1School of Molecular Biosciences
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)URF\R\211002MCSB - Plant Sciences
318499Diversity in STEMRucha KarnikThe Royal Society (ROYSOC)URF\R\211002School of Molecular Biosciences
173707Institutional Strategic Support Fund (2016)Anna DominiczakWellcome Trust (WELLCOTR)204820/Z/16/ZSchool of Cardiovascular & Metabolic Health