CaltechAUTHORS
  A Caltech Library Service

Phevamine A, a small molecule that suppresses plant immune responses

O’Neill, Erinn M. and Mucyn, Tatiana S. and Patteson, Jon B. and Finkel, Omri M. and Chung, Eui-Hwan and Baccile, Joshua A. and Massolo, Elisabetta and Schroeder, Frank C. and Dangl, Jeffery L. and Li, Bo (2018) Phevamine A, a small molecule that suppresses plant immune responses. Proceedings of the National Academy of Sciences of the United States of America, 115 (41). E9514-E9522. ISSN 0027-8424. http://resolver.caltech.edu/CaltechAUTHORS:20180920-144411925

[img] PDF - Published Version
Creative Commons Attribution Non-commercial No Derivatives.

1507Kb
[img] PDF - Supplemental Material
Creative Commons Attribution Non-commercial No Derivatives.

2354Kb
[img] MS Excel (Dataset_S01) - Supplemental Material
Creative Commons Attribution Non-commercial No Derivatives.

111Kb

Use this Persistent URL to link to this item: http://resolver.caltech.edu/CaltechAUTHORS:20180920-144411925

Abstract

Bacterial plant pathogens cause significant crop damage worldwide. They invade plant cells by producing a variety of virulence factors, including small-molecule toxins and phytohormone mimics. Virulence of the model pathogen Pseudomonas syringae pv. tomato DC3000 (Pto) is regulated in part by the sigma factor HrpL. Our study of the HrpL regulon identified an uncharacterized, three-gene operon in Pto that is controlled by HrpL and related to the Erwinia hrp-associated systemic virulence (hsv) operon. Here, we demonstrate that the hsv operon contributes to the virulence of Pto on Arabidopsis thaliana and suppresses bacteria-induced immune responses. We show that the hsv-encoded enzymes in Pto synthesize a small molecule, phevamine A. This molecule consists of L-phenylalanine, L-valine, and a modified spermidine, and is different from known small molecules produced by phytopathogens. We show that phevamine A suppresses a potentiation effect of spermidine and L-arginine on the reactive oxygen species burst generated upon recognition of bacterial flagellin. The hsv operon is found in the genomes of divergent bacterial genera, including ∼37% of P. syringae genomes, suggesting that phevamine A is a widely distributed virulence factor in phytopathogens. Our work identifies a small-molecule virulence factor and reveals a mechanism by which bacterial pathogens overcome plant defense. This work highlights the power of omics approaches in identifying important small molecules in bacteria–host interactions.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1803779115DOIArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1803779115/-/DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Baccile, Joshua A.0000-0003-4334-755X
Schroeder, Frank C.0000-0002-4420-0237
Li, Bo0000-0002-8019-8891
Additional Information:© 2018 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Sheng Yang He, Michigan State University, East Lansing, MI, and approved August 10, 2018 (received for review March 3, 2018) We thank Dr. Albert Bowers for helpful discussions of the manuscript, Dr. Gary Pielak for the naming of the phevamines, Dr. Jillian Tyrrell for cloning the hsv operon into the pLIC-His vector, Dr. Jake Malone for sharing the pBBR5 plasmid, Dr. Jim Jorgenson and Katherine Simpson for helpful discussion of isolation of phevamines, and Kevin Santa Maria for assistance with MultiGeneBlast. This work is supported by the Rita Allen Foundation and the David and Lucile Packard Foundation (B.L.), National Institutes of Health (R00 GM099904 to B.L., 5T32 GM008500 to J.A.B., and R01 GM112739-01 to F.C.S.), the National Science Foundation (IOS-1257373 to J.L.D.), and the Howard Hughes Medical Institute. J.L.D. is an Investigator of the Howard Hughes Medical Institute, and F.C.S. is a Faculty Scholar of the Howard Hughes Medical Institute. E.M.O. and T.S.M. contributed equally to this work. Author contributions: E.M.O., T.S.M., J.L.D., and B.L. designed research; E.M.O., T.S.M., J.B.P., O.M.F., and E.-H.C. performed research; J.B.P., O.M.F., J.A.B., E.M., and F.C.S. contributed new reagents/analytic tools; E.M.O., T.S.M., J.L.D., and B.L. analyzed data; and E.M.O., T.S.M., J.L.D., and B.L. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1803779115/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Rita Allen FoundationUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
NIHR00 GM099904
NIH Predoctoral Fellowship5T32 GM008500
NIHR01 GM112739-01
NSFIOS-1257373
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:natural products; genome mining; phytopathogen; virulence factor; plant immunity
Record Number:CaltechAUTHORS:20180920-144411925
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180920-144411925
Official Citation:Phevamine A, a small molecule that suppresses plant immune responses. Erinn M. O’Neill, Tatiana S. Mucyn, Jon B. Patteson, Omri M. Finkel, Eui-Hwan Chung, Joshua A. Baccile, Elisabetta Massolo, Frank C. Schroeder, Jeffery L. Dangl, Bo Li. Proceedings of the National Academy of Sciences Oct 2018, 115 (41) E9514-E9522; DOI: 10.1073/pnas.1803779115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:89811
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:20 Sep 2018 22:08
Last Modified:09 Oct 2018 17:26

Repository Staff Only: item control page