Genome‐wide association identifies a BAHD acyltransferase activity that assembles an ester of glucuronosylglycerol and phenylacetic acid

Simpson, Jeffrey P.; Kim, Colin Y.; Kaur, Amanpreet; Weng, Jing‐Ke; Dilkes, Brian; Chapple, Clint

doi:10.1111/tpj.16737

Title: Genome‐wide association identifies a BAHD acyltransferase activity that assembles an ester of glucuronosylglycerol and phenylacetic acid

Journal Article · 31 March 2024 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.16737 · OSTI ID:2331512

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Department of Biochemistry Purdue University West Lafayette Indiana 47907 USA, Purdue Center for Plant Biology West Lafayette Indiana 47907 USA
Whitehead Institute for Biomedical Research Cambridge Massachusetts 02142 USA, Department of Biological Engineering Massachusetts Institute of Technology Cambridge Massachusetts 02139 USA, Department of Molecular and Cellular Biology Harvard University Cambridge Massachusetts 02138 USA
Whitehead Institute for Biomedical Research Cambridge Massachusetts 02142 USA, Department of Chemistry and Chemical Biology &, Department of Bioengineering Northeastern University Boston Massachusetts 02120 USA, Institute for Plant‐Human Interface Northeastern University Boston Massachusetts 02120 USA

SUMMARY Genome‐wide association studies (GWAS) are an effective approach to identify new specialized metabolites and the genes involved in their biosynthesis and regulation. In this study, GWAS of Arabidopsis thaliana soluble leaf and stem metabolites identified alleles of an uncharacterized BAHD‐family acyltransferase (AT5G57840) associated with natural variation in three structurally related metabolites. These metabolites were esters of glucuronosylglycerol, with one metabolite containing phenylacetic acid as the acyl component of the ester. Knockout and overexpression of AT5G57840 in Arabidopsis and heterologous overexpression in Nicotiana benthamiana and Escherichia coli demonstrated that it is capable of utilizing phenylacetyl‐CoA as an acyl donor and glucuronosylglycerol as an acyl acceptor. We, thus, named the protein Glucuronosylglycerol Ester Synthase (GGES). Additionally, phenylacetyl glucuronosylglycerol increased in Arabidopsis CYP79A2 mutants that overproduce phenylacetic acid and was lost in knockout mutants of UDP‐sulfoquinovosyl: diacylglycerol sulfoquinovosyl transferase, an enzyme required for glucuronosylglycerol biosynthesis and associated with glycerolipid metabolism under phosphate‐starvation stress. GGES is a member of a well‐supported clade of BAHD family acyltransferases that arose by duplication and neofunctionalized during the evolution of the Brassicales within a larger clade that includes HCT as well as enzymes that synthesize other plant‐specialized metabolites. Together, this work extends our understanding of the catalytic diversity of BAHD acyltransferases and uncovers a pathway that involves contributions from both phenylalanine and lipid metabolism.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0020368

OSTI ID:: 2331512

Alternate ID(s):: OSTI ID: 2331513; OSTI ID: 2339571

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 6 Vol. 118; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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