SlREM1 Triggers Cell Death by Activating an Oxidative Burst and Other Regulators

Plant Physiol. 2020 Jun;183(2):717-732. doi: 10.1104/pp.20.00120. Epub 2020 Apr 21.

Abstract

Programmed cell death (PCD), a highly regulated feature of the plant immune response, involves multiple molecular players. Remorins (REMs) are plant-specific proteins with varied biological functions, but their function in PCD and plant defense remains largely unknown. Here, we report a role for remorin in disease resistance, immune response, and PCD regulation. Overexpression of tomato (Solanum lycopersicum) REMORIN1 (SlREM1) increased susceptibility of tomato to the necrotrophic fungus Botrytis cinerea and heterologous expression of this gene triggered cell death in Nicotiana benthamiana leaves. Further investigation indicated that amino acids 173 to 187 and phosphorylation of SlREM1 played key roles in SlREM1-triggered cell death. Intriguingly, multiple tomato REMs induced cell death in N benthamiana leaves. Yeast two-hybrid, split luciferase complementation, and coimmunoprecipitation assays all demonstrated that remorin proteins could form homo- and heterocomplexes. Using isobaric tags for relative and absolute quantitative proteomics, we identified that some proteins related to cell death regulation, as well as N benthamiana RESPIRATORY BURST OXIDASE HOMOLOG B (which is essential for reactive oxygen species production), were notably upregulated in SlREM1-expressing leaves. Heterologous expression of SlREM1 increased reactive oxygen species accumulation and triggered other cell death regulators. Our findings indicate that SlREM1 is a positive regulator of plant cell death and provide clues for understanding the PCD molecular regulatory network in plants.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Botrytis / pathogenicity
  • Cell Death / genetics
  • Cell Death / physiology*
  • Disease Resistance / genetics
  • Disease Resistance / physiology
  • Gene Expression Regulation, Plant / genetics
  • Gene Expression Regulation, Plant / physiology
  • Nicotiana / metabolism
  • Nicotiana / microbiology
  • Plant Diseases / microbiology
  • Plant Leaves / metabolism
  • Plant Leaves / microbiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Reactive Oxygen Species / metabolism
  • Respiratory Burst / genetics
  • Respiratory Burst / physiology*
  • Solanum lycopersicum / metabolism
  • Solanum lycopersicum / microbiology

Substances

  • Plant Proteins
  • Reactive Oxygen Species
  • remorin

Supplementary concepts

  • Botrytis cinerea