Salicylic acid is a key player of Arabidopsis autophagy mutant susceptibility to the necrotrophic bacterium Dickeya dadantii

Martine Rigault,Alia Dellagi,Sylvie Citerne,Céline Masclaux-Daubresse

doi:10.1038/s41598-021-83067-6

Abstract

Autophagy is a ubiquitous vesicular process for protein and organelle recycling in eukaryotes. In plant, autophagy is reported to play pivotal roles in nutrient recycling, adaptation to biotic and abiotic stresses. The role of autophagy in plant immunity remains poorly understood. Several reports showed enhanced susceptibility of different Arabidopsis autophagy mutants (atg) to necrotrophic fungal pathogens. Interaction of necrotrophic bacterial pathogens with autophagy is overlooked. We then investigated such interaction by inoculating the necrotrophic enterobacterium Dickeya dadantii in leaves of the atg2 and atg5 mutants and an ATG8a overexpressing line. Overexpressing ATG8a enhances plant tolerance to D. dadantii. While atg5 mutant displayed similar susceptibility to the WT, the atg2 mutant exhibited accelerated leaf senescence and enhanced susceptibility upon infection. Both phenotypes were reversed when the sid2 mutation, abolishing SA signaling, was introduced in the atg2 mutant. High levels of SA signaling in atg2 mutant resulted in repression of the jasmonic acid (JA) defense pathway known to limit D. dadantii progression in A. thaliana. We provide evidence that in atg2 mutant, the disturbed hormonal balance leading to higher SA signaling is the main factor causing increased susceptibility to the D. dadantii necrotroph by repressing the JA pathway and accelerating developmental senescence.

Highlights

Autophagy is a ubiquitous vesicular process for protein and organelle recycling in eukaryotes
The role of autophagy in Arabidopsis tolerance to necrotrophic phytopathogens was only reported for fungal plant pathogens (Table 1), using atg mutants or transgenic lines over-expressing ATGgenes
To know whether autophagy is involved in Arabidopsis tolerance to bacterial necrotrophs, we addressed the issue with the model bacterial necrotroph Dickeya dadantii[60]

Summary

Introduction

Autophagy is a ubiquitous vesicular process for protein and organelle recycling in eukaryotes. Defense-related responses involve protein phosphorylation, accumulation of reactive oxygen species (ROS), ionic fluxes and biosynthesis of phytohormones leading to transcriptional activation of genes coding for enzymes involved in the synthesis of antimicrobial compounds such as phytoalexins or pathogenesis related (PR) proteins[1,2,3,4,5,6] To activate these defenses, plants are equipped with receptors that can detect different types of molecules either derived from the pathogen or derived from their own tissues[7,8,9]. The ATG2 protein is involved in lipid recruitment for autophagosome membrane elongation Both ATG5 and ATG2 are encoded by single genes and their mutants display strong senescence and limited-growth phenotypes phenotypes are more severe in atg[2] than in atg[532–35]. Autophagy genes are up-regulated under stress conditions, amongst which plant infection by p athogens[39,40]

Methods

Results

Conclusion