Can autophagy enhance crop resilience to environmental stress?

Abstract

Climate change imposes abiotic stress on plants, significantly threatening global agriculture and food security. This indicates a need to apply our understanding of plant stress responses to improve crop resilience to these threats. Stress damages critical cellular components such as mitochondria, chloroplasts and the endoplasmic reticulum. Left unmitigated, abiotic stress can lead to cell death, which typically decreases overall plant health and productivity. Autophagy is a catabolic process that maintains cellular homeostasis by degrading and recycling damaged and dysfunctional cell components and organelles. Importantly, autophagy promotes plant tolerance to a wide range of environmental stresses, and manipulation of autophagy may lead to improved stress resilience in crops. Here, we discuss recent advances in our understanding of how autophagy affects abiotic stress resistance. We discuss the function of autophagy in different abiotic stresses (including nutrient stress, salt stress, drought, heat, cold, hypoxia, light stress and combined stresses) and provide insights from functional and genome-wide transcriptomic studies. We also evaluate the potential to enhance crop survival and productivity in suboptimal environmental conditions by activating autophagy, emphasizing the importance of targeted manipulation of key genes involved in the autophagy pathway.This article is part of the theme issue 'Crops under stress: can we mitigate the impacts of climate change on agriculture and launch the 'Resilience Revolution'?'.

Keywords: autophagy; autophagy manipulation; crop improvement; stress response.

Figure 1.

Role of autophagy in plant responses to abiotic stresses. (A) Plants experience a range of abiotic stresses, including heat, cold, water scarcity, high salinity, nutrient deficiency, excessive light, UV radiation, waterlogging and submergence, all of which ultimately affect plant growth and development. (B) Abiotic stresses can cause damage to cellular components, such as membranes, proteins and organelles, leading to disruptions in normal physiological functions. (C) In response to abiotic stresses, plants activate stress signalling pathways including those mediated by brassinosteroids (BR), abscisic acid (ABA), salicylic acid (SA), ethylene (ETH) and reactive oxygen species (ROS), that subsequently activate the autophagy pathway. (D) Autophagy aids in managing cellular damage and maintaining homeostasis by facilitating the degradation and recycling of damaged cell components. (E) This process ultimately enhances plant survival, increases tolerance of abiotic stresses and improves growth, development and yield.

Figure 2.

Stacked bar plot showing percentages of 43 core autophagy-related (ATG) genes that are upregulated, downregulated or remain unchanged in the indicated stress condition from GSE93420 (C starvation) [93,170] and GSE147962 (all other stresses) [169] expression datasets. Asterisks (${\displaystyle \ast }$) indicate stress conditions in which >50% of ATG genes are significantly upregulated. Plus sign (+) indicates stress conditions in which 25–50% of ATG genes are significantly upregulated. C starvation, carbon starvation; Cd, cadmium; HL, high light; HS, heat stress; PQ, Paraquat.

Figure 3.

Strategic approach to enhance abiotic stress resilience in crops by targeting autophagy. (A) The process begins with the identification of key autophagy-related genes in extremophiles and/or selected crop species, providing a foundation for understanding stress responses. (B) Following gene identification, functional studies are conducted at multiple levels, including genome, transcriptome, proteome and metabolome, to elucidate the roles of these genes in stress responses. (C) A model of the autophagy regulatory network is then developed to integrate the findings and visualize interactions among key components. (D) This model guides the generation and screening of transgenic plants in crops of interest, aimed at enhancing their autophagy pathways. (E) This approach culminates in increased abiotic stress tolerance in these crops, achieved without adverse effects on growth or yield and thereby supporting sustainable agricultural practices.