Engineering of benzoxazinoid biosynthesis in Arabidopsis thaliana: Metabolic and physiological challenges. (December 2021)

• Record Type: Journal Article
• Authors: Abramov, Aleksej; Hoffmann, Thomas; Stark, Timo D.; Zheng, Linlin; Lenk, Stefan; Hammerl, Richard; Lanzl, Tobias; Dawid, Corinna; Schön, Chris-Carolin; Schwab, Wilfried; Gierl, Alfons; Frey, Monika
• Is Part Of: Phytochemistry. Volume 192(2021)
• Publication Date: 2021-12
• Subjects: Arabidopsis thaliana (Brassicaceae) -- Zea mays (Poaceae) -- Benzoxazinones -- Chemical defence -- Indolinone -- Phytotoxicity -- Metabolic stress -- Transgenic pathway -- Bioengineering -- Pathway evolution; Botanical chemistry -- Periodicals; Biochemistry -- Periodicals; Botany -- Periodicals; Chimie végétale -- Périodiques; 572.2
• DOI: 10.1016/j.phytochem.2021.112947
• Languages: English
• ISSNs: 0031-9422

Abstract

Abstract: Plant specialised metabolites constitute a layer of chemical defence. Classes of the defence compounds are often restricted to a certain taxon of plants, e.g. benzoxazinoids (BX) are characteristically detected in grasses. BXs confer wide-range defence by controlling herbivores and microbial pathogens and are allelopathic compounds. In the crops maize, wheat and rye high concentrations of BXs are synthesised at an early developmental stage. By transfer of six Bx -genes ( Bx1 to Bx5 and Bx8 ) it was possible to establish the biosynthesis of 2, 4-dihydroxy-1, 4-benzoxazin-3-one glucoside (GDIBOA) in a concentration of up to 143 nmol/g dry weight in Arabidopsis thaliana . Our results indicate that inefficient channeling of substrates along the pathway and metabolisation of intermediates in host plants might be a general drawback for transgenic establishment of specialised metabolite biosynthesis pathways. As a consequence, BX levels required for defence are not obtained in Arabidopsis. We could show that indolin-2-one (ION), the first specific intermediate, is phytotoxic and is metabolised by hydroxylation and glycosylation by a wide spectrum of plants. In Arabidopsis, metabolic stress due to the enrichment of ION leads to elevated levels of salicylic acid (SA) and in addition to its intrinsic phytotoxicity, ION affects plant morphology indirectly via SA. We could show that Bx3 has a crucial role in the evolution of the pathway, first based on its impact on flux into the pathway and, second by C3-hydroxylation of the phytotoxic ION. Thereby BX3 interferes with a supposedly generic detoxification system towards the non-specific intermediate. Graphical abstract: Benzoxazinoid biosynthesis in transgenic Arabidopsis is impaired by modification of intermediates leading to metabolic stress. Image 1 Highlights: Transfer of six maize genes enabled benzoxazinoid (BX) biosynthesis in Arabidopsis. The phytotoxic BX pathway intermediate indolinone causes morphological changes. Plants detoxify indolinone by hydroxylation and glucosylation. Metabolisation of indolinone and content of salicylic acid are interdependent. Acquisition of BX3 function might be a prerequisite in the evolution of the pathway.