Persistent fatty acid catabolism during plant oil synthesis

Authors: KOLEY, SOMNATH - Donald Danforth Plant Science Center; JYOTI, POONAM - Donald Danforth Plant Science Center; LINGWAN, MANEESH - Donald Danforth Plant Science Center; WEI, MICHAEL - Donald Danforth Plant Science Center; XU, CHUNHUI - University Of Missouri; CHU, KEVN - Donald Danforth Plant Science Center; WILLIAMS, RUSSELL - Donald Danforth Plant Science Center; KOO, ABRAHAM - Donald Danforth Plant Science Center; THELAN, JAY - Donald Danforth Plant Science Center; XU, DONG - University Of Missouri; Allen, Douglas

Submitted to: Cell Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2025
Publication Date: 3/29/2025
Citation: Koley, S., Jyoti, P., Lingwan, M., Wei, M., Xu, C., Chu, K.L., Williams, R.B., Koo, A.J., Thelan, J.J., Allen, D.K., Xu, D. 2025. Persistent fatty acid catabolism during plant oil synthesis. Cell. 44(4). https://doi.org/10.1016/j.celrep.2025.115492.
DOI: https://doi.org/10.1016/j.celrep.2025.115492

Interpretive Summary: Lipids are energy dense and a form of renewable energy for biotechnological applications such as biofuels that can supplant petroleum, and equally important to human and animal diets. While the presence of lipids can serve many important plant functions, including as a signal molecule, or to provide a protective barrier, or as membranes that define organelles, the most concentrated location of lipids is in seeds, where storage lipids are produced as an energy reserve that is needed when seedlings grow during germination. The accumulation of reserves, including lipids, in seeds is thought to be a stable process. We show quantitatively, that lipids in seeds as well as leaves and other parts of the plant are turned over, broken down for other needs, and importantly this process takes place in a different subcellular location than has been previously considered. The location has implications for the cell operation. Our understanding of, what seems like a futile cycle of biosynthesis and breakdown, is clearly incomplete. If we want to make more lipids in seeds for the benefit of humankind, then we need to understand these processes so that we can reduce lipid breakdown and maximize the levels for biotech applications and human and animal consumption. Further, our results indicate that the enhanced turnover of lipids in lines engineered to make more lipid, may partially explain why efforts to engineer oilseeds have not met expectations.

Technical Abstract: Plant lipids are an essential energy source for diets and are a sustainable alternative to petroleum-based fuels and feedstocks. Fatty acid breakdown during seed germination is crucial for seedling establishment but unexpected during seed filling. Here, we demonstrate that the simultaneous biosynthesis and degradation of fatty acids begins early and continues across all phases of oil filling and throughout the photoperiod. Tests in camelina, rapeseed, and an engineered high-oil tobacco line confirmed that concomitant synthesis and breakdown in oil-producing tissues over development is the rule rather than the exception. Furthermore, we show that transgenics, designed to elevate fatty acid biosynthesis, failed to achieve anticipated increases in storage lipid levels due to increased degradation, potentially explaining the underperformance of engineered lines compared to expectations more generally.