skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

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.

Authors:
 [1];  [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [1];  [2]
  1. Washington Univ., St. Louis, MO (United States)
  2. The Ohio State Univ., Columbus, OH (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1498334
Grant/Contract Number:  
AC02-06CH11357; IOS-1030250; IOS-1645908; DBI-1427621
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 14; Journal Issue: 1; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; Pseudomonas syringae; auxins; plant bacterial pathogens; plant pathogens; Arabidopsis thaliana; aldehydes; crystal structure; pathogenesis

Citation Formats

McClerklin, Sheri A., Lee, Soon Goo, Harper, Christopher P., Nwumeh, Ron, Jez, Joseph M., Kunkel, Barbara N., and Mackey, David. Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000. United States: N. p., 2018. Web. doi:10.1371/journal.ppat.1006811.
McClerklin, Sheri A., Lee, Soon Goo, Harper, Christopher P., Nwumeh, Ron, Jez, Joseph M., Kunkel, Barbara N., & Mackey, David. Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000. United States. https://doi.org/10.1371/journal.ppat.1006811
McClerklin, Sheri A., Lee, Soon Goo, Harper, Christopher P., Nwumeh, Ron, Jez, Joseph M., Kunkel, Barbara N., and Mackey, David. Tue . "Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000". United States. https://doi.org/10.1371/journal.ppat.1006811. https://www.osti.gov/servlets/purl/1498334.
@article{osti_1498334,
title = {Indole-3-acetaldehyde dehydrogenase-dependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000},
author = {McClerklin, Sheri A. and Lee, Soon Goo and Harper, Christopher P. and Nwumeh, Ron and Jez, Joseph M. and Kunkel, Barbara N. and Mackey, David},
abstractNote = {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.},
doi = {10.1371/journal.ppat.1006811},
url = {https://www.osti.gov/biblio/1498334}, journal = {PLoS Pathogens},
issn = {1553-7374},
number = 1,
volume = 14,
place = {United States},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 28 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response
journal, February 2006


Salicylic Acid Inhibits Pathogen Growth in Plants through Repression of the Auxin Signaling Pathway
journal, October 2007


Achieving Diversity in the Face of Constraints: Lessons from Metabolism
journal, June 2012


Structure-Based Mutational Studies of Substrate Inhibition of Betaine Aldehyde Dehydrogenase BetB from Staphylococcus aureus
journal, April 2014


Auxin Production Is a Common Feature of Most Pathovars of Pseudomonas syringae
journal, February 1998


Auxin: Regulation, Action, and Interaction
journal, February 2005


Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion
journal, May 1997


Role and structural characterization of plant aldehyde dehydrogenases from family 2 and family 7
journal, May 2015


Indole-3-acetic acid in microbial and microorganism-plant signaling
journal, July 2007


COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine
journal, May 2008


Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism
journal, September 2011


A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling
journal, April 2006


CorR Regulates Multiple Components of Virulence in Pseudomonas syringae pv. tomato DC3000
journal, July 2006


Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology
journal, December 2007


GH3-mediated Auxin Homeostasis Links Growth Regulation with Stress Adaptation Response in Arabidopsis
journal, February 2007


Auxin and Plant-Microbe Interactions
journal, November 2010


Isochorismate synthase is required to synthesize salicylic acid for plant defence
journal, November 2001


The Conjugated Auxin Indole-3-Acetic Acid–Aspartic Acid Promotes Plant Disease Development
journal, February 2012


The plant immune system
journal, November 2006


Characterization of Phenylpyruvate Decarboxylase, Involved in Auxin Production of Azospirillum brasilense
journal, August 2007


Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria
journal, September 2012


The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000
journal, August 2003


Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes.
journal, July 1986


Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress
journal, March 2013


An improved suicide vector for construction of chromosomal insertion mutations in bacteria
journal, September 1992


HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes
journal, July 2006


Research Notes Cloning of the Genes for Indoleacetic Acid Synthesis from Pseudomonas syringae pv. syringae
journal, January 1991


Features and development of Coot
journal, March 2010


JAZing up jasmonate signaling
journal, February 2008


The main auxin biosynthesis pathway in Arabidopsis
journal, October 2011


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010


Aldehyde dehydrogenase (ALDH) superfamily in plants: gene nomenclature and comparative genomics
journal, September 2012


Differential Involvement of Indole-3-Acetic Acid Biosynthetic Pathways in Pathogenicity and Epiphytic Fitness of Erwinia herbicola pv. gypsophilae
journal, July 1998


Identification and Characterization of a Well-Defined Series of Coronatine Biosynthetic Mutants of Pseudomonas syringae pv. tomato DC3000
journal, February 2004


Indole-3-acetic acid in plant–microbe interactions
journal, January 2014


Some chemical and physiological properties of 3-indolylpyruvic acid
journal, September 1956


Auxin Biosynthesis and Its Role in Plant Development
journal, June 2010


The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana
journal, November 2005


Coenzyme Isomerization Is Integral to Catalysis in Aldehyde Dehydrogenase ,
journal, June 2003


A liquid chromatography–tandem mass spectrometry-based assay for indole-3-acetic acid–amido synthetase
journal, July 2009


Phaser crystallographic software
journal, July 2007


Auxin activity: Past, present, and future
journal, February 2015


Generation and Characterization of Tn5 Insertion Mutations in Pseudomonas syringae pv. tomato
journal, January 1986


    Works referencing / citing this record:

    Xanthomonas translucens commandeers the host rate-limiting step in ABA biosynthesis for disease susceptibility
    journal, October 2019


    Dynamic pigmentary and structural coloration within cephalopod chromatophore organs
    journal, March 2019


    Why Do Herbivorous Mites Suppress Plant Defenses?
    journal, July 2018