Methionine catabolism in Arabidopsis cells is initiated by a γ-cleavage process and leads to S-methylcysteine and isoleucine syntheses

• Published in: Proceedings of the National Academy of Sciences - PNAS 2006-10, Vol.103 (42), p.15687-15692
• Main Authors: Rébeillé, F, Jabrin, S, Bligny, R, Loizeau, K, Gambonnet, B, Wilder, V. van, Douce, R, Ravanel, S
• Format: Article
• Language: English
• Subjects: 5-methylcysteine; adenosylmethionine; Alkynes - metabolism; amino acid metabolism; Amino acids; Arabidopsis - cytology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Biological Sciences; carbon-sulfur lyases; Carbon-Sulfur Lyases - genetics; Carbon-Sulfur Lyases - metabolism; Catabolism; Cell growth; cell lines; Cellular metabolism; Complementary DNA; cysteine; Cysteine - analogs & derivatives; Cysteine - biosynthesis; enzyme activity; Enzymes; gene expression; Glycine - analogs & derivatives; Glycine - metabolism; isoleucine; Isoleucine - biosynthesis; Messenger RNA; methionine; Methionine - metabolism; methionine gamma-lyase; Molecules; Nuclear Magnetic Resonance, Biomolecular; Plant cells; Protein metabolism; Sulfonylurea Compounds - metabolism
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0606195103

Despite recent progress in elucidating the regulation of methionine (Met) synthesis, little is known about the catabolism of this amino acid in plants. In this article, we present several lines of evidence indicating that the cleavage of Met catalyzed by Met γ-lyase is the first step in this process. First, we cloned an Arabidopsis cDNA coding a functional Met γ-lyase (AtMGL), a cytosolic enzyme catalyzing the conversion of Met into methanethiol, α-ketobutyrate, and ammonia. AtMGL is present in all of the Arabidopsis organs and tissues analyzed, except in quiescent dry mature seeds, thus suggesting that AtMGL is involved in the regulation of Met homeostasis in various situations. Also, we demonstrated that the expression of AtMGL was induced in Arabidopsis cells in response to high Met levels, probably to bypass the elevated Km of the enzyme for Met. Second, [13C]-NMR profiling of Arabidopsis cells fed with [13C]Met allowed us to identify labeled S-adenosylmethionine, S-methylmethionine, S-methylcysteine (SMC), and isoleucine (Ile). The unexpected production of SMC and Ile was directly associated to the function of Met γ-lyase. Indeed, we showed that part of the methanethiol produced during Met cleavage could react with an activated form of serine to produce SMC. The second product of Met cleavage, α-ketobutyrate, entered the pathway of Ile synthesis in plastids. Together, these data indicate that Met catabolism in Arabidopsis cells is initiated by a γ-cleavage process and can result in the formation of the essential amino acid Ile and a potential storage form for sulfide or methyl groups, SMC.