Combating stress: the interplay between hormone signaling and autophagy in plants

Abstract

Autophagy is a conserved recycling process in which cellular components are delivered to and degraded in the vacuole/lysosome for reuse. In plants, it assists in responding to dynamic environmental conditions and maintaining metabolite homeostasis under normal or stress conditions. Under stress, autophagy is activated to remove damaged components and to recycle nutrients for survival, and the energy sensor kinases target of rapamycin (TOR) and SNF-related kinase 1 (SnRK1) are key to this activation. Here, we discuss accumulating evidence that hormone signaling plays critical roles in regulating autophagy and plant stress responses, although the molecular mechanisms by which this occurs are often not clear. Several hormones have been shown to regulate TOR activity during stress, in turn controlling autophagy. Hormone signaling can also regulate autophagy gene expression, while, reciprocally, autophagy can regulate hormone synthesis and signaling pathways. We highlight how the interplay between major energy sensors, plant hormones, and autophagy under abiotic and biotic stress conditions can assist in plant stress tolerance.

Autophagy in plants: Physiological roles and post‐translational regulation

“…Accumulating findings suggest that plant autophagy is regulated by hormone signaling at the transcriptional and posttranslational levels in response to various environmental stresses (Gou et al, 2019; Signorelli et al, 2019; Liao and Bassham, 2020). Specifically, the abscisic acid (ABA) signaling pathway is likely involved in autophagy‐mediated stress responses.…”

Autophagy Dances with Phytohormones upon Multiple Stresses

“…Conversely, the ABA-activated SnRK2 can phosphorylate RAPTOR, thus inhibiting TOR-mediated autophagy [ 84 ]. These studies revealed that crosstalk between autophagy and ABA signaling is mediated by the phosphorylation modification of corresponding regulators [ 17 ]. GA antagonistically interplays with ABA in multiple biological processes, but little has been known about this antagonism in regulating autophagy.…”

“…A recent study has shown that a high level of SA caused autophagy-mediated PCD in apple, and the phenotype of accelerated PCD during senescence and immunity in atatg5 mutant was through the SA-dependent rather than the intact JA or ET signaling pathway [ 49 ]. Similar to SA, JA also participates in response to various biotic stresses, and the JA-related WRKY genes have already been implicated as mediating autophagy gene expression upon heat stress and fungal pathogen infection [ 17 ]. For example, WRKY33 was not only involved in the JA-mediated signaling pathway to regulate plant resistance to necrotrophic fungal pathogens, but also directly interacted with ATG18a to regulate autophagy in Arabidopsis [ 17 , 91 ], suggesting WRKY33 coordinates the JA signaling and autophagy pathway to regulate the pathogen stress.…”

“…Phytohormones play important roles in plant growth, development, and abiotic and biotic stress responses. Briefly, abscisic acid (ABA), ethylene (ET), jasmonic acid (JA), and salicylic acid (SA) were generally known to directly regulate stress responses in plants, while auxin, cytokinin (CK), gibberellin (GA), and brassinolide (BR) modulate broad physiological effects through their corresponding signaling transduction in response to stresses [ 8 , 17 ]. Although the crosstalk between autophagy and hormone signaling upon stress has been described recently [ 8 , 17 ], the detailed regulatory mechanism is still poorly understood.…”

“…Briefly, abscisic acid (ABA), ethylene (ET), jasmonic acid (JA), and salicylic acid (SA) were generally known to directly regulate stress responses in plants, while auxin, cytokinin (CK), gibberellin (GA), and brassinolide (BR) modulate broad physiological effects through their corresponding signaling transduction in response to stresses [ 8 , 17 ]. Although the crosstalk between autophagy and hormone signaling upon stress has been described recently [ 8 , 17 ], the detailed regulatory mechanism is still poorly understood. Genome-wide analysis of the TaATG promoter in bread wheat identified numerous ABA-, IAA-, GA-, ET-, MeJA-, and SA-related cis -elements, as well as others related to light, anoxic, heat, cold, drought, and wound stresses [ 18 ].…”