Mechanistic basis for the emergence of EPS1 as a catalyst in salicylic acid biosynthesis of Brassicaceae

Michael P. Torrens-Spence, Jason O. Matos, Tianjie Li, David W. Kastner, Colin Y. Kim, Ziqi Wang, Christopher M. Glinkerman, Jennifer Sherk, Heather J. Kulik, Yi Wang and Jing-Ke Weng ()
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Michael P. Torrens-Spence: Whitehead Institute for Biomedical Research
Jason O. Matos: Whitehead Institute for Biomedical Research
Tianjie Li: The Chinese University of Hong Kong
David W. Kastner: Massachusetts Institute of Technology
Colin Y. Kim: Whitehead Institute for Biomedical Research
Ziqi Wang: The Chinese University of Hong Kong
Christopher M. Glinkerman: Whitehead Institute for Biomedical Research
Jennifer Sherk: Whitehead Institute for Biomedical Research
Heather J. Kulik: Massachusetts Institute of Technology
Yi Wang: The Chinese University of Hong Kong
Jing-Ke Weng: Whitehead Institute for Biomedical Research

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract Salicylic acid (SA) production in Brassicaceae plants is uniquely accelerated from isochorismate by EPS1, a newly identified enzyme in the BAHD acyltransferase family. We present crystal structures of EPS1 from Arabidopsis thaliana in both its apo and substrate-analog-bound forms. Integrating microsecond-scale molecular dynamics simulations with quantum mechanical cluster modeling, we propose a pericyclic rearrangement lyase mechanism for EPS1. We further reconstitute the isochorismate-derived SA biosynthesis pathway in Saccharomyces cerevisiae, establishing an in vivo platform to examine the impact of active-site residues on EPS1 functionality. Moreover, stable transgenic expression of EPS1 in soybean increases basal SA levels, highlighting the enzyme’s potential to enhance defense mechanisms in non-Brassicaceae plants lacking an EPS1 ortholog. Our findings illustrate the evolutionary adaptation of an ancestral enzyme’s active site to enable a novel catalytic mechanism that boosts SA production in Brassicaceae plants.

Date: 2024
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DOI: 10.1038/s41467-024-54437-1

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