Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds

Abstract

Sulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, iron, zinc and manganese remobilizations from the rosette to the seeds in Arabidopsis thaliana. Here, we have compared the role of autophagy in sulphur and nitrogen management at the whole plant level, performing concurrent labelling with 34S and 15N isotopes on atg5 mutants and control lines. We show that both 34S and 15N remobilizations from the rosette to the seeds are impaired in the atg5 mutants irrespective of salicylic acid accumulation and of sulphur nutrition. The comparison in each genotype of the partitions of 15N and 34S in the seeds (as % of the whole plant) indicates that the remobilization of 34S to the seeds was twice more efficient than that of 15N in both autophagy mutants and control lines under high S conditions, and also in control lines under low S conditions. This was different in the autophagy mutants grown under low S conditions. Under low S, the partition of 34S to their seeds was indeed not twice as high but similar to that of 15N. Such discrepancy shows that when sulphate availability is scarce, autophagy mutants display stronger defects for 34S remobilization relative to 15N remobilization than under high S conditions. It suggests, moreover, that autophagy mainly affects the transport of N-poor S-containing molecules and possibly sulphate.

Autophagy in plants: Physiological roles and post‐translational regulation

“…Autophagy is also involved in recycling of micronutrients, such as zinc and sulfur in plant cells (Eguchi et al, 2017; Lornac et al, 2020; Tarnowski et al, 2020). In Arabidopsis , zinc limitation induces the accumulation of autophagosomes (Eguchi et al, 2017).…”

“…More recently, two independent studies uncovered an indispensable role of autophagy in sulfur metabolism. (Lornac et al, 2020) observed that in the Arabidopsis atg5 mutants, the remobilization of sulfur from rosettes to seeds is compromised. Furthermore, the selective autophagy receptor NBR1 is likely important for plant responses to sulfur deficiency (Tarnowski et al, 2020), suggesting that selective autophagy may improve the efficiency of micronutrient remobilization from the vacuole.…”

The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants

“…Although there are no other data on sulfur metabolism and its homeostasis in autophagy mutants, we could assume similar mechanisms. Further studies revealed the role of autophagy in sulfur management at the whole plant level by the application of 34 S isotope labeling on atg5 mutant and wild type plants [126]. Sulfur remobilization from the rosette to seed was impaired in atg5 mutant and most of the amino acids, including methionine and cysteine, accumulated in the rosette leaves of atg5 mutant, irrespective of sulfur supply.…”

Genome-Wide Identification of CsATGs in Tea Plant and the Involvement of CsATG8e in Nitrogen Utilization

“…Recently, Chen et al [ 28 ] have shown that the overexpression of AtATG8s ( AtATG8a , AtATG8e , AtATG8f and AtATG8g ) with different promoters enhanced autophagosome number, promoted autophagy activity and increased the N remobilization efficiency under optimal N conditions without a negative effect on yield or biomass. Besides N, autophagy is also involved in recycling other nutrients, such as iron, zinc, manganese and sulfur [ 29 , 30 , 31 ]. Despite the characterization of the involvement of ATG8s in N remobilization and the participation of autophagy in recycling other nutrients in a number of plant species, little is known about them in tea plant.…”