Disruption of the plant-specific CFS1 gene impairs autophagosome turnover and triggers EDS1-dependent cell death

Arpaporn Sutipatanasomboon,Anke Y Zienert,Swen Schellmann,Martin Hülskamp,Gerrit J K Praefcke,Mojgan Shahriari,Mojgan Shahriari,Ellen G Alwood,Birger Marin,Silke Robatzek,Silke Robatzek,Stefanie Herberth,Britta Müller,Heidrun Häweker,Heidrun Häweker,Kathryn R Ayscough

doi:10.1038/s41598-017-08577-8

Abstract

Cell death, autophagy and endosomal sorting contribute to many physiological, developmental and immunological processes in plants. They are mechanistically interconnected and interdependent, but the molecular basis of their mutual regulation has only begun to emerge in plants. Here, we describe the identification and molecular characterization of CELL DEATH RELATED ENDOSOMAL FYVE/SYLF PROTEIN 1 (CFS1). The CFS1 protein interacts with the ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT I (ESCRT-I) component ELCH (ELC) and is localized at ESCRT-I-positive late endosomes likely through its PI3P and actin binding SH3YL1 Ysc84/Lsb4p Lsb3p plant FYVE (SYLF) domain. Mutant alleles of cfs1 exhibit auto-immune phenotypes including spontaneous lesions that show characteristics of hypersensitive response (HR). Autoimmunity in cfs1 is dependent on ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)-mediated effector-triggered immunity (ETI) but independent from salicylic acid. Additionally, cfs1 mutants accumulate the autophagy markers ATG8 and NBR1 independently from EDS1. We hypothesize that CFS1 acts at the intersection of autophagosomes and endosomes and contributes to cellular homeostasis by mediating autophagosome turnover.

Highlights

Cell death is an important process for plant development and responses to stress[1]
Signals generated from coiled-coiled (CC)-nucleotide-binding leucine-rich repeat receptor proteins (NB-LRRs) are mediated by NON RACE-SPECIFIC DISEASE RESISTANCE (NDR1); whereas signals generated from Toll-interleukin-1-receptor domain (TIR)-NB-LRRs are mediated by ENHANCED DISEASE SUSCEPTIBILITY (EDS1)[7]
One striking feature in the N-terminal part is the presence of a conserved PSAPP motif in CELL DEATH RELATED ENDOSOMAL FYVE/SYLF PROTEIN 1 (CFS1) that is absent from At1g29800 (Figs 1 and S2A)

Summary

Introduction

Cell death is an important process for plant development and responses to stress[1]. Different types of cell death have been classified based on morphological and biochemical criteria[2, 3]. Necrosis is a form of an acute cell death that often results from environmental stress It is characterized by swelling of mitochondria, production of reactive oxygen species, and early rupture of the plasma membrane leading to protoplast shrinkage. ETI is activated when a pathogen unloads virulent effectors with the aim to suppress PTI and invade the cell[5] These effectors are recognized by intracellular nucleotide-binding leucine-rich repeat receptor proteins (NB-LRRs) or resistance (R)-gene products directly or indirectly by guarding effector-modified host targets[6]. Several mutants of genes involved in autophagy are sensitive to nutrient-limiting conditions and display early senescence[17,18,19] It was demonstrated in Picea abies embryonic suspensor that inhibition of autophagy partially contributes to the switch from vacuolar to necrotic cell death[20]. Autophagosomes can fuse with multivesicular bodies (MVBs), forming amphisomes before vacuolar degradation[21]

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Results

Conclusion