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Title: Divergent evolution of extreme production of variant plant monounsaturated fatty acids

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [1];  [3];  [4]; ORCiD logo [5];  [5];  [6]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [3];  [3];  [9];  [2];  [2]; ORCiD logo [1]
  1. US Department of Energy Center for Advanced Bioenergy and Bioproducts Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, NE 68588
  2. Department of Biology, Brookhaven National Laboratory, Upton, NY 11973
  3. Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68588
  4. Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, Department of Computer Science and Engineering, University of Nebraska-Lincoln, Lincoln, NE 68588
  5. Biochemistry &, Cell Biology Department, Stony Brook University, Stony Brook, NY 11794
  6. National Key Lab of Crop Genetic Improvement and College of Plant Science and Technology, Huazhong Agricultural University, 430070 Wuhan, China
  7. Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, NE 68588
  8. Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, Department of Agronomy &, Horticulture, University of Nebraska-Lincoln, Lincoln, NE 68588
  9. Department of Pharmacognosy and Pharmaceutical Botany, Excellent Research Laboratory, Phytomedicine and Pharmaceutical Biotechnology Excellence Center, Faculty of Pharmaceutical Sciences, Prince of Songkla University, 91110 Songkla, Thailand

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.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States); Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)
Grant/Contract Number:
SC0018420; KC0304000; SC0012704; IOS-13-39385; P30GM133893
OSTI ID:
1877745
Alternate ID(s):
OSTI ID: 1877092; OSTI ID: 1996360
Report Number(s):
BNL-223177-2022-JAAM; e2201160119
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 119 Journal Issue: 30; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

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