Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000

Sheri A McClerklin; Soon Goo Lee; Christopher P Harper; Ron Nwumeh; Joseph M Jez; Barbara N Kunkel

doi:10.1371/journal.ppat.1006811

Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000

PLoS Pathog. 2018 Jan 2;14(1):e1006811. doi: 10.1371/journal.ppat.1006811. eCollection 2018 Jan.

Authors

Sheri A McClerklin¹, Soon Goo Lee¹, Christopher P Harper¹, Ron Nwumeh¹, Joseph M Jez¹, Barbara N Kunkel¹

Affiliation

¹ Department of Biology, Washington University, St. Louis, Missouri, United States of America.

Abstract

The bacterial pathogen Pseudomonas syringae modulates plant hormone signaling to promote infection and disease development. P. syringae uses several strategies to manipulate auxin physiology in Arabidopsis thaliana to promote pathogenesis, including its synthesis of indole-3-acetic acid (IAA), the predominant form of auxin in plants, and production of virulence factors that alter auxin responses in the host; however, the role of pathogen-derived auxin in P. syringae pathogenesis is not well understood. Here we demonstrate that P. syringae strain DC3000 produces IAA via a previously uncharacterized pathway and identify a novel indole-3-acetaldehyde dehydrogenase, AldA, that functions in IAA biosynthesis by catalyzing the NAD-dependent formation of IAA from indole-3-acetaldehyde (IAAld). Biochemical analysis and solving of the 1.9 Å resolution x-ray crystal structure reveal key features of AldA for IAA synthesis, including the molecular basis of substrate specificity. Disruption of aldA and a close homolog, aldB, lead to reduced IAA production in culture and reduced virulence on A. thaliana. We use these mutants to explore the mechanism by which pathogen-derived auxin contributes to virulence and show that IAA produced by DC3000 suppresses salicylic acid-mediated defenses in A. thaliana. Thus, auxin is a DC3000 virulence factor that promotes pathogenicity by suppressing host defenses.

Publication types

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

MeSH terms

Aldehyde Oxidoreductases / chemistry
Aldehyde Oxidoreductases / genetics
Aldehyde Oxidoreductases / metabolism
Aldehyde Oxidoreductases / physiology*
Arabidopsis / genetics
Arabidopsis / metabolism
Arabidopsis / microbiology*
Binding Sites
Gene Expression Regulation, Plant
Host-Pathogen Interactions / genetics
Indoleacetic Acids / metabolism*
Indoles / metabolism*
Organisms, Genetically Modified
Plant Diseases / genetics
Plant Diseases / microbiology
Pseudomonas Infections / genetics
Pseudomonas Infections / microbiology
Pseudomonas syringae / genetics
Pseudomonas syringae / metabolism
Pseudomonas syringae / pathogenicity*
Virulence* / genetics

Substances

Indoleacetic Acids
Indoles
indole-3-acetaldehyde
indoleacetic acid
Aldehyde Oxidoreductases
aldehyde dehydrogenase (NAD(P)+)

Grants and funding

This work was supported by grants from the National Science Foundation (IOS-1030250 and IOS-1645908 awarded to BNK and MCB-115771 and MCB-1614539 awarded to JMJ). Information about the IOS and MCB programs can be found at http://www.nsf.gov/dir/index.jsp?org=BIO. Acquisition of the QTRAP LC-MS/MS used for hormone analysis was funded by National Science Foundation Grant No. DBI-1427621 to the DDPSC. Portions of this research were carried out at the Argonne National Laboratory Structural Biology Center of the Advanced Photon Source, a national user facility operated by the University of Chicago for the Department of Energy Office of Biological and Environmental Research (DE-AC02-06CH11357). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.