Divergent evolution of extreme production of variant plant monounsaturated fatty acids

Abstract

Metabolic extremes provide opportunities to understand enzymatic and metabolic plasticity and biotechnological tools for novel biomaterial production. We discovered that seed oils of many Thunbergia species contain up to 92% of the unusual monounsaturated petroselinic acid (18:1Δ6), one of the highest reported levels for a single fatty acid in plants. Supporting the biosynthetic origin of petroselinic acid, we identified a Δ6-stearoyl-acyl carrier protein (18:0-ACP) desaturase from Thunbergia laurifolia , closely related to a previously identified Δ6-palmitoyl-ACP desaturase that produces sapienic acid (16:1Δ6)-rich oils in Thunbergia alata seeds. Guided by a T. laurifolia desaturase crystal structure obtained in this study, enzyme mutagenesis identified key amino acids for functional divergence of Δ6 desaturases from the archetypal Δ9-18:0-ACP desaturase and mutations that result in nonnative enzyme regiospecificity. Furthermore, we demonstrate the utility of the T. laurifolia desaturase for the production of unusual monounsaturated fatty acids in engineered plant and bacterial hosts. Through stepwise metabolic engineering, we provide evidence that divergent evolution of extreme petroselinic acid and sapienic acid production arises from biosynthetic and metabolic functional specialization and enhanced expression of specific enzymes to accommodate metabolism of atypical substrates.

Boosting plant oil yields: the role of genetic engineering in industrial applications

“…These FA can be converted to adipic acid (C6:0), a building block of 6,6-nylon, with an annual production of about 2.5 million metric tonnes in the petrochemical industry. Overexpression of related acyl-ACP desaturase has resulted in very low levels of these monounsaturated FA (Gan et al, 2022).…”

A comparison of natural and induced diversity in plant oils

“…In addition to the already cited examples of the detection of nebraskanic and wuhanic acids in (Li et al, 2018), an analysis of the leaf lipidome has also yielded 393 molecular species within 23 different lipid classes (Tarazona et al, 2015) that cannot be deduced from the FA composition alone. A very recent article (Gan et al, 2022) report on the exploration of Thunbergia genus, which revealed that numerous species accumulate petroselenic (18:1 D6 ) instead of sapienic acid (16:1 D6 ). Thus, detailed study of a genus may reveal the accumulation of unexpected FAs, resulting from probable evolutionary divergence in the genus.…”

Editorial: Metabolic engineering of valuable compounds in photosynthetic organisms

“…Photosynthetic organisms, including plants and algae, possess a remarkable ability to harness carbon dioxide and solar energy, enabling them to produce a vast array of complex compounds such as phenolic acids ( Zhou et al., 2021 ), terpenes ( Miller et al., 2020 ), unsaturated fatty acids ( Kokabi et al., 2020 ; Gan et al., 2022 ), and other lipid products ( Zienkiewicz and Zienkiewicz, 2020 ). This inherent capability positions them as highly promising platforms for the sustainable production of valuable biomolecules.…”