Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization

Proc Natl Acad Sci U S A. 2019 Oct 15;116(42):21274-21284. doi: 10.1073/pnas.1911892116. Epub 2019 Oct 1.

Abstract

Plasmodesmata (PD) are plant-specific membrane-lined channels that create cytoplasmic and membrane continuities between adjacent cells, thereby facilitating cell-cell communication and virus movement. Plant cells have evolved diverse mechanisms to regulate PD plasticity in response to numerous environmental stimuli. In particular, during defense against plant pathogens, the defense hormone, salicylic acid (SA), plays a crucial role in the regulation of PD permeability in a callose-dependent manner. Here, we uncover a mechanism by which plants restrict the spreading of virus and PD cargoes using SA signaling by increasing lipid order and closure of PD. We showed that exogenous SA application triggered the compartmentalization of lipid raft nanodomains through a modulation of the lipid raft-regulatory protein, Remorin (REM). Genetic studies, superresolution imaging, and transmission electron microscopy observation together demonstrated that Arabidopsis REM1.2 and REM1.3 are crucial for plasma membrane nanodomain assembly to control PD aperture and functionality. In addition, we also found that a 14-3-3 epsilon protein modulates REM clustering and membrane nanodomain compartmentalization through its direct interaction with REM proteins. This study unveils a molecular mechanism by which the key plant defense hormone, SA, triggers membrane lipid nanodomain reorganization, thereby regulating PD closure to impede virus spreading.

Keywords: Remorin; SA-controlled lipid order; membrane nanodomain compartmentalization; plasmodesmata closure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / metabolism
  • Arabidopsis Proteins / metabolism
  • Cell Communication / physiology
  • Cell Membrane / metabolism
  • Glucans / metabolism
  • Membrane Lipids / metabolism*
  • Membrane Microdomains / metabolism
  • Plant Cells / metabolism
  • Plant Growth Regulators / metabolism
  • Plant Proteins / metabolism*
  • Plasmodesmata / metabolism*
  • Salicylic Acid / metabolism*
  • Signal Transduction / physiology

Substances

  • Arabidopsis Proteins
  • Glucans
  • Membrane Lipids
  • Plant Growth Regulators
  • Plant Proteins
  • remorin
  • callose
  • Salicylic Acid