Ionic stress enhances ER–PM connectivity via phosphoinositide-associated SYT1 contact site expansion in Arabidopsis

Eunkyoung Lee, Steffen Vanneste, Jessica Pérez-Sancho, Francisco Benitez-Fuente, Matthew Strelau, Alberto P. Macho, Miguel A. Botella, Jiří Friml, and Abel Rosado
PNAS January 22, 2019 116 (4) 1420-1429; published ahead of print January 22, 2019 https://doi.org/10.1073/pnas.1818099116

  1. Edited by June B. Nasrallah, Cornell University, Ithaca, NY, and approved December 6, 2018 (received for review October 23, 2018)

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Significance

Interorganelle connectivity and nonvesicular information transfer are hallmarks of biological systems. These processes facilitate communication between organelles, allowing them to adapt to changing cellular environments. In plants, the endoplasmic reticulum (ER)–plasma membrane (PM) contact sites (EPCSs) physically connect the cortical ER and the PM, and act as general platforms for Ca2+ homeostasis regulation and the cellular adaptation to environmental stresses. Our identification of ionic stress and PM phosphoinositides as enhancers of ER–PM connectivity advances our understanding of how stress influences interorganelle communication. Furthermore, our analyses of the spatiotemporal regulation of EPCS expansion highlights unique mechanisms that plants activate to maintain interorganelle communication during long-term exposure to environmental stress, not described in other eukaryotes.

Abstract

The interorganelle communication mediated by membrane contact sites (MCSs) is an evolutionary hallmark of eukaryotic cells. MCS connections enable the nonvesicular exchange of information between organelles and allow them to coordinate responses to changing cellular environments. In plants, the importance of MCS components in the responses to environmental stress has been widely established, but the molecular mechanisms regulating interorganelle connectivity during stress still remain opaque. In this report, we use the model plant Arabidopsis thaliana to show that ionic stress increases endoplasmic reticulum (ER)–plasma membrane (PM) connectivity by promoting the cortical expansion of synaptotagmin 1 (SYT1)-enriched ER–PM contact sites (S-EPCSs). We define differential roles for the cortical cytoskeleton in the regulation of S-EPCS dynamics and ER–PM connectivity, and we identify the accumulation of phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] at the PM as a molecular signal associated with the ER–PM connectivity changes. Our study highlights the functional conservation of EPCS components and PM phosphoinositides as modulators of ER–PM connectivity in eukaryotes, and uncovers unique aspects of the spatiotemporal regulation of ER–PM connectivity in plants.

Footnotes

  • ↵1Present address: Instituto de Hortofruticultura Subtropical y Mediterránea, Universidad de Málaga-Consejo Superior de Investigaciones Científicas, Departamento de Biología Molecular y Bioquímica, Facultad de Ciencias, Universidad de Málaga, 29071 Málaga, Spain.

  • ↵2To whom correspondence should be addressed. Email: abel.rosado{at}botany.ubc.ca.

  • Author contributions: A.R. designed research; E.L., J.P.-S., F.B.-F., M.S., and A.P.M. performed research; S.V. and A.P.M. contributed new reagents/analytic tools; E.L., S.V., J.P.-S., M.A.B., J.F., and A.R. analyzed data; and A.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1818099116/-/DCSupplemental.

Published under the PNAS license.

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Ionic stress enhances ER–PM connectivity via phosphoinositide-associated SYT1 contact site expansion in Arabidopsis
Eunkyoung Lee, Steffen Vanneste, Jessica Pérez-Sancho, Francisco Benitez-Fuente, Matthew Strelau, Alberto P. Macho, Miguel A. Botella, Jiří Friml, Abel Rosado
Proceedings of the National Academy of Sciences Jan 2019, 116 (4) 1420-1429; DOI: 10.1073/pnas.1818099116
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