Arabidopsis γ-glutamylcyclotransferase affects glutathione content and root system architecture during sulfur starvation

• Published in: The New phytologist 2019-02, Vol.221 (3), p.1387-1397
• Main Authors: Joshi, Naveen C., Meyer, Andreas J., Bangash, Sajid A. K., Zheng, Zhi-Liang, Leustek, Thomas
• Format: Article
• Language: English
• Subjects: Amino acids; Arabidopsis - drug effects; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - drug effects; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Buthionine Sulfoximine - pharmacology; Coding; Computer architecture; Cysteine; Cysteine - metabolism; Depletion; DNA, Bacterial - genetics; gamma-Glutamylcyclotransferase - genetics; gamma-Glutamylcyclotransferase - metabolism; Gene Expression Regulation, Plant - drug effects; Genes; Glutamic Acid - metabolism; Glutathione; Glutathione - metabolism; Glycine; Glycine (amino acid); Meristem - metabolism; Models, Biological; Mutants; Mutation - genetics; nutrient foraging; Phenotype; Plant Roots - drug effects; Plant Roots - growth & development; Plant Roots - metabolism; Plant tissues; Promoter Regions, Genetic - genetics; RNA, Messenger - genetics; RNA, Messenger - metabolism; root system architecture; Roots; Seedlings; Starvation; Sulfates; Sulfur; sulfur (S); Sulfur - deficiency; Sulphur; Tissue; Transcription; γ-Glutamylcyclotransferase; γ‐glutamyl‐cyclotransferase
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.15466

• γ-Glutamylcyclotransferase initiates glutathione degradation to component amino acids L-glutamate, L-cysteine and L-glycine. The enzyme is encoded by three genes in Arabidopsis thaliana, one of which (GGCT2;1) is transcriptionally upregulated by starvation for the essential macronutrient sulfur (S). Regulation by S-starvation suggests that GGCT2;1 mobilizes L-cysteine from glutathione when there is insufficient sulfate for de novo L-cysteine synthesis. • The response of wild-type seedlings to S-starvation was compared to ggct2;1 null mutants. • S-starvation causes glutathione depletion in S-starved wild-type seedlings, but higher glutathione is maintained in the primary root tip than in other seedling tissues. Although GGCT2;1 is induced throughout seedlings, its expression is concentrated in the primary root tip where it activates the γ-glutamyl cycle. S-starved wild-type plants also produce longer primary roots, and lateral root growth is suppressed. While glutathione is also rapidly depleted in ggct2;1 null seedlings, much higher glutathione is maintained in the primary root tip compared to the wild-type. S-starved ggct2;1 primary roots grow longer than the wild-type, and lateral root growth is not suppressed. • These results point to a role for GGCT2;1 in S-starvation-response changes to root system architecture through activity of the γ-glutamyl cycle in the primary root tip. L-Cysteine mobilization from glutathione is not solely a function of GGCT2;1.