Metabolic diversification of nitrogen‐containing metabolites by the expression of a heterologous lysine decarboxylase gene in Arabidopsis. (27th August 2019)

• Record Type: Journal Article
• Authors: Shimizu, Yohei; Rai, Amit; Okawa, Yuko; Tomatsu, Hajime; Sato, Masaru; Kera, Kota; Suzuki, Hideyuki; Saito, Kazuki; Yamazaki, Mami
• Is Part Of: Plant journal. Volume 100:Number 3(2019)
• Page Start: 505
• Page End: 521
• Publication Date: 2019-08-27
• Subjects: lysine decarboxylase -- cadaverine catabolism -- Arabidopsis thaliana -- chemodiversity -- non‐targeted metabolome analysis -- Lys‐derived alkaloids; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.14454
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: Lysine decarboxylase converts l ‐lysine to cadaverine as a branching point for the biosynthesis of plant Lys‐derived alkaloids. Although cadaverine contributes towards the biosynthesis of Lys‐derived alkaloids, its catabolism, including metabolic intermediates and the enzymes involved, is not known. Here, we generated transgenic Arabidopsis lines by expressing an exogenous lysine/ornithine decarboxylase gene from Lupinus angustifolius ( La‐L/ODC ) and identified cadaverine‐derived metabolites as the products of the emerged biosynthetic pathway. Through untargeted metabolic profiling, we observed the upregulation of polyamine metabolism, phenylpropanoid biosynthesis and the biosynthesis of several Lys‐derived alkaloids in the transgenic lines. Moreover, we found several cadaverine‐derived metabolites specifically detected in the transgenic lines compared with the non‐transformed control. Among these, three specific metabolites were identified and confirmed as 5‐aminopentanal, 5‐aminopentanoate and δ‐valerolactam. Cadaverine catabolism in a representative transgenic line (DC29) was traced by feeding stable isotope‐labeled [α‐ 15 N]‐ or [ε‐ 15 N]‐l ‐lysine. Our results show similar 15 N incorporation ratios from both isotopomers for the specific metabolite features identified, indicating that these metabolites were synthesized via the symmetric structure of cadaverine. We propose biosynthetic pathways for the metabolites on the basis of metabolite chemistry and enzymes known or identified through catalyzing specific biochemical reactions in this study. Our study shows that this pool of enzymes with promiscuous activities is the driving force for metabolite diversification in plants. Thus, this study not only provides valuable information for understanding the catabolic mechanism of cadaverine but also demonstrates that cadaverine accumulation is one of the factors to expand plant chemodiversity, which may lead to the emergence of Lys‐derived alkaloid biosynthesis. Significance Statement: Cadaverine, a reaction product of lysine decarboxylase, serves as an intermediate of plant Lys‐derived alkaloids. Despite being an important metabolite in the expansion of plant chemodiversity, little is known about its catabolism in planta . In this study, we identified cadaverine‐derived metabolites and their metabolic pathways in transgenic Arabidopsis, which will provide a molecular basis for understanding the emergence of chemodiversity through cadaverine production.