A Pathogen-Responsive Gene Cluster for Highly Modified Fatty Acids in Tomato

Ju Eun Jeon; Jung-Gun Kim; Curt R Fischer; Niraj Mehta; Cosima Dufour-Schroif; Kimberly Wemmer; Mary Beth Mudgett; Elizabeth Sattely

doi:10.1016/j.cell.2019.11.037

A Pathogen-Responsive Gene Cluster for Highly Modified Fatty Acids in Tomato

Cell. 2020 Jan 9;180(1):176-187.e19. doi: 10.1016/j.cell.2019.11.037.

Authors

Ju Eun Jeon¹, Jung-Gun Kim², Curt R Fischer³, Niraj Mehta⁴, Cosima Dufour-Schroif⁵, Kimberly Wemmer⁵, Mary Beth Mudgett⁶, Elizabeth Sattely⁷

Affiliations

¹ Department of Chemical Engineering, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.
² Department of Biology, Stanford University, Stanford, CA 94305, USA.
³ Stanford ChEM-H (Chemistry, Engineering, and Medicine for Human Health), Stanford University, Stanford, CA 94305, USA.
⁴ Department of Chemistry, Stanford University, Stanford, CA 94305, USA.
⁵ L'Oreal, Paris, France.
⁶ Department of Biology, Stanford University, Stanford, CA 94305, USA. Electronic address: [email protected].
⁷ Department of Chemical Engineering, Stanford University, Stanford, CA 94305, USA; Howard Hughes Medical Institute, Stanford, CA 94305, USA. Electronic address: [email protected].

Abstract

In response to biotic stress, plants produce suites of highly modified fatty acids that bear unusual chemical functionalities. Despite their chemical complexity and proposed roles in pathogen defense, little is known about the biosynthesis of decorated fatty acids in plants. Falcarindiol is a prototypical acetylenic lipid present in carrot, tomato, and celery that inhibits growth of fungi and human cancer cell lines. Using a combination of untargeted metabolomics and RNA sequencing, we discovered a biosynthetic gene cluster in tomato (Solanum lycopersicum) required for falcarindiol production. By reconstituting initial biosynthetic steps in a heterologous host and generating transgenic pathway mutants in tomato, we demonstrate a direct role of the cluster in falcarindiol biosynthesis and resistance to fungal and bacterial pathogens in tomato leaves. This work reveals a mechanism by which plants sculpt their lipid pool in response to pathogens and provides critical insight into the complex biochemistry of alkynyl lipid production.

Keywords: acetylenase; acetylenic lipids; antifungal oxylipin; falcarindiol; plant lipid gene cluster; plant natural product biosynthesis; transcriptomics; untargeted metabolomics.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Disease Resistance / genetics
Diynes / chemistry
Diynes / metabolism*
Fatty Acids / biosynthesis*
Fatty Acids / metabolism
Fatty Alcohols / chemistry
Fatty Alcohols / metabolism*
Gene Expression Regulation, Plant / genetics
Metabolomics
Multigene Family / genetics
Plant Diseases / microbiology
Plant Leaves / metabolism
Plant Proteins / metabolism
Plants, Genetically Modified
Solanum lycopersicum / genetics*
Stress, Physiological / genetics

Substances

Diynes
Fatty Acids
Fatty Alcohols
Plant Proteins
falcarindiol

Grants and funding

U01 GM110699/GM/NIGMS NIH HHS/United States