Autophagy in plants

Abstract

Autophagy is a process of cellular self-eating, which allows organisms to eliminate and recycle unwanted components and damaged organelles to maintain cellular homeostasis. It is an important process in the development of eukaryotic organisms. Autophagy plays a critical role in many physiological processes in plants such as nutrient remobilization, cell death, immunity, and abiotic stress responses. Autophagy thus represents an obvious target for generating resilient crops. During plant development, autophagy is also implicated in the differentiation and maturation of various cell types and plant organs, including root cap cells, tracheary elements, gametes, fruits and seeds. Here, we review our current understanding and recent advances of plant autophagy including insight into autophagy regulation and signaling as well as autophagosome membrane biogenesis. In addition, we describe how autophagy contributes to development, metabolism, biotic and abiotic stress tolerance and where the autophagic field is heading in terms of applied research for crop improvement.

Keywords: Plant autophagy; cargo receptors; crop improvement; development; endomembrane trafficking; immunity; metabolism; quality control; regulation and signalling; stress tolerance.

Figure 1.

Overview of the autophagy pathway and the major mechanisms regulating the autophagy core machinery in plants. Plant genomes contain more than 40 ATG genes that encode the functional units of the autophagy machinery to drive autophagosome biogenesis. Autophagosomes are initiated at ER-localised preautophagosomal structures (phagophore assembly sites, PAS) and mature after recruitment of cellular content to the expanding phagophore. Upon autophagosomal fusion with the vacuole, the sequestered cargo is released for lytic degradation and subsequent recycling. Transcription factors (purple) activate or repress ATG genes in response to environmental or endogenous cues. Protein kinases and phosphatases (orange) modify autophagy core components to control their activity. Post-translational modifications (grey) of autophagy proteins by persulfidation inhibit or by acetylation activate autophagy. Stability of the autophagy machinery is modulated by ubiquitination and subsequent degradation (blue). See text for details.

Figure 2.

Updated interactions between the endomembrane system and autophagosome biogenesis in plants. The plant endomembrane system contains multiple membrane-bound organelles including the endoplasmic reticulum (ER), the Golgi apparatus (GA), trans-Golgi network/early endosome (TGN/EE), multivesicular body/prevacuolar compartment/late endosome (MVB/PVC/LE), and vacuole. The endomembrane system contributes to autophagosome biogenesis via multiple new mechanisms or pathways (A-F) for subsequent autophagosome-vacuole fusion and degradation in plants, with mechanistic details highlighted in the corresponding enlarged boxes shown below. (A) Autophagosome biogenesis is regulated by AtEH/Pan1, F-actin and endocytic machinery at the ER-PM contact site (EPCS) for the degradation of endocytic components in Arabidopsis. (B) The Arabidopsis ORP2A coordinates with both the ER residential VAP27-1 and ATG8 on the autophagosome to mediate ER-autophagosomal MCS for autophagosome biogenesis. (C) The Arabidopsis SNARE family proteins AtVAMP724/AtVAMP726 regulate the trafficking of ATG9 vesicles. (D) Distinct AtSAR1d-positive COPII population is formed to regulate autophagic flux via the AtSAR1D-AtRABD2a nexus. FYVE2 interacts with AtSar1b and ATG18-ATG2 complex to regulate autophagosome biogenesis. (F) Phosphorylated FREE1 coordinates with both the ESCRT and ATG machinery to mediate autophagosome closure in Arabidopsis. (G) CFS1 interacts with ATG8 and VPS23A in mediating autophagosome-MVB fusion to facilitate the formation of amphisome.

Figure 3.

Examples of selective autophagy targeting proteins, organelles, and pathogens in plants. (A) During drought or carbon starvation BIN2 phosphorylates DSK2 which targets BES1 to ATG8 for subsequent autophagic degradation. (B) Upon immune activation MPK3 phosphorylates Exo70B2 which binds to ATG8. (C) Ubiquitinated proteasome binds RPN10 under proteotoxic stress or nitrogen starvation leading to proteophagy. (D) Photodamaged chloroplast gets ubiquitinated leading to chlorophagy. (E) NBR1 targets ABI transcription factors for autophagic degradation when overexpressed. (F) NBR1 targets the capsid protein P4 and entire viral particle leading to xenophagy of cauliflower mosaic virus (CaMV). See text for details.

Figure 4.

The contribution of autophagy to abiotic stress tolerance in plants. The figure summarizes the observed effects of altered autophagy levels on abiotic stress tolerance in different plant species. Autophagy inhibition was achieved by loss-of-function mutations in ATG genes and the NBR1 cargo receptor or by chemical means. Autophagy activation was mediated by overexpression (OE) of ATG, NBR1 and other genes, as well as loss-of-function mutations in negative autophagy regulators or chemical treatment. See text for details. The figure was created with BioRender.com.

Figure 5.

Overview of known functions of autophagy in immunity and disease, and strategies of pathogens to manipulate autophagy processes for their own benefit. Autophagy plays a dual role in the regulation of the immunity-related hypersensitive response (HR) upon infection with various pathogens and suppresses disease-related cell death of necroptrophic fungi. Selective autophagy pathways target viral proteins and particles as well as bacterial effector proteins for degradation. Furthermore, autophagosomes are diverted towards haustoria to mediate focal defence responses against an oomycete pathogen, and autophagy mechanisms are involved in the activation of jasmonic acid (JA)-dependent defences against nematodes. In contrast, cytoprotective functions of autophagy benefit infection by increasing host cell survival, and selective autophagy pathways are hijacked by pathogens to eliminate defence components and to target the proteasome involved in salicylic-dependent immune responses. Autophagic structures are also likely involved in nutrient diversion to the haustorial feeding sites of oomycetes and promote formation of viral replication complexes. Pathogens are able to manipulate autophagy processes by various strategies. These include effector-mediated interactions with and/or modifications of ATG proteins and autophagy regulators as well as interruption of vacuolar functions required for autophagic cargo degradation. Autophagy levels are also modulated by fungal secretion of secondary metabolites. See text for further details.