Discontinuous fatty acid elongation yields hydroxylated seed oil with improved function

Abstract

The biosynthesis of ‘unusual’ fatty acids with structures that deviate from the common C16 and C18 fatty acids has evolved numerous times in the plant kingdom. Characterization of unusual fatty acid biosynthesis has enabled increased understanding of enzyme substrate properties, metabolic plasticity and oil functionality. Here, we report the identification of a novel pathway for hydroxy fatty acid biosynthesis based on the serendipitous discovery of two C24 fatty acids containing hydroxyl groups at the 7 and 18 carbon atoms as major components of the seed oil of Orychophragmus violaceus, a China-native Brassicaceae. Biochemical and genetic evidence are presented for premature or ‘discontinuous’ elongation of a 3-OH intermediate by a divergent 3-ketoacyl-CoA (coenzyme A) synthase during a chain extension cycle as the origin of the 7-OH group of the dihydroxy fatty acids. Tribology studies revealed superior high-temperature lubricant properties for O. violaceus seed oil compared to castor oil, a high-performance vegetable oil lubricant. These findings provide a direct pathway for designing a new class of environmentally friendly lubricants and unveil the potential of O. violaceus as a new industrial oilseed crop.

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Fig. 1: O. violaceus flowers, seeds and seed oil analyses.
Fig. 2: GC-MS analysis of unusual fatty acids in O. violaceus seeds.
Fig. 3: Elucidation of the structures of the very-long-chain dihydroxy fatty acids from O. violaceus seed oil.
Fig. 4: Analysis of FAMEs of Arabidopsis seeds engineered to express OvFAD2-2 alone or in combination with OvFAE1-1 and/or OvFAE1-2.
Fig. 5: Comparison of lubricative properties of cold-pressed O. violaceus (Ov oil) and castor oil (Castor oil).
Fig. 6: Proposed biosynthetic pathway for nebraskanic acid.

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Acknowledgements

We thank the National Natural Science Foundation of China (grant number 31370286) and Fundamental Research Funds for the Central Universities (programme number 2662015PY12) for support to C.Z. and the National Science Foundation (Plant Genome IOS-13-39385) and Huazhong Agricultural University Scientific and Technological Self-Innovation Foundation (programme number 2015RC010) for support to E.B.C. NMR and LC/MS instrumentation at IUPUI were acquired with funding from the NSF (grant numbers CHE-0619254 and DBI-0821661, R.E.M.). A.M.T. appreciates support of the NSF (MCB-0919938, R.E.M.) and the Department of Chemistry and Chemical Biology, IUPUI. We thank M.Morton (University of Nebraska-Lincoln) for assistance with preliminary NMR studies, S.Stymne and J.Lindberg Yilmaz (ScanBiRes) for conducting fatty acid elongation assays, and E.Moriyama and A.Voshall (University of Nebraska-Lincoln) for transcriptome assembly and mining.

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X.L., A.M.T., K.D.C., D.B., C.Z., R.E.M. and E.B.C. designed the research. X.L., A.M.T., A.S., J.L., R.E.C., W.Z., L.B., C.Z., R.E.M. and E.B.C. performed the research. Z.L. provided novel research materials and contributed to the research conception. X.L., A.M.T., J.L., R.E.C., K.D.C., D.B., C.Z., R.E.M. and E.B.C. analysed the data. X.L., A.M.T., J.L., K.D.C, D.B., C.Z., R.E.M. and E.B.C. wrote the manuscript.

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Correspondence to Chunyu Zhang or Robert E. Minto or Edgar B. Cahoon.

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Li, X., Teitgen, A.M., Shirani, A. et al. Discontinuous fatty acid elongation yields hydroxylated seed oil with improved function. Nature Plants 4, 711–720 (2018). https://doi.org/10.1038/s41477-018-0225-7

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