Identification of triacylglycerol remodeling mechanism to synthesize unusual fatty acid containing oils

Authors: PARCHURI, PRASAD - Washington State University; BHANDARI, SAJINA - Washington State University; AZEEZ, ABDUL - Washington State University; Chen, Grace; Johnson, Kumiko; Shockey, Jay; SMERTENKO, ANDREI - Washington State University; BATES, PHILIP - Washington State University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2024
Publication Date: 4/26/2024
Citation: Parchuri, P., Bhandari, S., Azeez, A., Chen, G., Johnson, K., Shockey, J., Smertenko, A., Bates, P.D. 2024. Identification of triacylglycerol remodeling mechanism to synthesize unusual fatty acid containing oils. Nature Communications. 15. Article 3547. https://doi.org/10.1038/s41467-024-47995-x.
DOI: https://doi.org/10.1038/s41467-024-47995-x

Interpretive Summary: Oils produced from oilseed crops such as cotton, canola, and soybean represent one of the most lucrative potential sources of future food, feed, and fuel, which will become increasingly important as the world population grows and the amount of tillable land shrinks. To best control the types and amounts of oils produced by these plants, much more must be learned about the underlying genetics and biochemistry that controls the composition of seed oils. Most plants produce oils as an endpoint of metabolism as seeds mature. Here we report an exception to that rule. The desert crop lesquerella makes high levels of industrially useful fatty acids in its oils, but does so by remodeling the otherwise 'endpoint' oil molecules in its seeds after their initial synthesis is complete. The genes that produce the enzymes that carry out this unique pathway are described here.

Technical Abstract: Typical plant membranes and storage lipids are comprised of five common fatty acids yet over 450 unusual fatty acids accumulate in seed oils of various plant species. Plant oils are important human and animal nutrients, while some unusual fatty acids such as hydroxylated fatty acids (HFA) are used within the chemical industry (lubricants, paints, polymers, cosmetics, etc.). Most unusual fatty acids are extracted from non-agronomic crops leading to high production costs. Attempts to engineer HFA into crops are unsuccessful due to bottlenecks in the overlapping pathways of oil and membrane lipid synthesis where HFA are not compatible. Physaria fendleri naturally overcomes these bottlenecks through a novel triacylglycerol (TAG) remodeling mechanism where HFA are incorporated into TAG after initial synthesis. TAG remodeling involves a novel TAG lipase and two diacylglycerol acyltransferases (DGAT) that are selective for different stereochemical and acyl-containing species of diacylglycerol within a synthesis, partial degradation, and resynthesis cycle. The TAG lipase interacts with DGAT1, localizes to the endoplasmic reticulum (with the DGATs) but also spots around the lipid droplet, likely forming a TAG remodeling metabolon near the lipid droplet ER junction. Each characterized DGAT and TAG lipase is able to increase HFA accumulation in engineered seed oils.