Many roads lead to autophagy: the connection between sulfur metabolism and autophagy during metal stress in plants

Abstract

During plant development and in response to stress conditions, autophagy contributes to the intracellular degradation of cellular components and subsequent nutrient recycling. As this process is highly connected to the nutrient status of the plant, autophagy also contributes to the mobilization of sulfur from source to sink tissues as well as the maintenance of primary sulfate assimilation. In turn, sulfur signals regulate autophagy, with sulfide (an intermediate of primary sulfate assimilation) exerting a repressive effect and sulfur deficiency having a stimulatory effect. In addition to a sulfur deficiency response in the plant resulting from low external sulfate availability, stresses such as metal exposure also perturb sulfur metabolism and can induce a 'functional sulfur deficiency' response through a surge in the production of thiol-rich metal chelators. As autophagy is increasingly linked to metal stress responses, this review proposes potential pathways through which metal-induced autophagy is linked to perturbations in sulfur metabolism, focusing on redox alterations and sucrose non-fermenting 1 (SNF1)-related kinase (SnRK)/target of rapamycin (TOR)-mediated nutrient signalling. Lastly, the connection between plant stress tolerance, autophagy and sulfur status is also discussed in terms of potential valorization strategies to maximize plant growth on metal-contaminated soils. This work provides an overview of the relationship between sulfur metabolism and autophagy, and explores how sulfur-related redox alterations and nutrient signalling may contribute to metal-induced autophagy.