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.

Plant pathogens have evolved several strategies to manipulate the biology of their hosts to facilitate colonization, growth to high levels in plant tissue, and production of disease. One of the less well known of these strategies is the synthesis of plant hormones and hormone analogs, and there is growing evidence that modulation of host hormone signaling is important during pathogenesis. Several plant pathogens produce the auxin indole-3-acetic acid (IAA) and/or virulence factors that modulate host auxin signaling. Auxin is well known for being involved in many aspects of plant growth and development, but recent findings have revealed that elevated IAA levels or enhanced auxin signaling can also promote disease development in some plant-pathogen interactions. In addition to stimulating plant cell growth during infection by gall-forming bacteria, auxin and auxin signaling can antagonize plant defense responses. Auxin can also act as a microbial signaling molecule to impact the biology of some pathogens directly. In this review, we summarize recent progress towards elucidating the roles that auxin production, modification of host auxin signaling, and direct effects of auxin on pathogens play during pathogenesis, with emphasis on the impacts of auxin on interactions with bacterial pathogens.

ABSTRACTModification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen Pseudomonas syringae strain PtoDC3000 produces the plant hormone auxin (Indole-3-acetic acid, or IAA) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth, demonstrating that host auxin signaling is required for normal susceptibility to PtoDC3000, and this phenotype was dependent on SA-mediated defenses. However, despite exhibiting decreased auxin perception, tir1 afb1 afb4 afb5 quadruple mutant plants lacking four of the six known auxin co-receptors supported increased levels of bacterial growth. This mutant also exhibited elevated IAA levels, suggesting that the increased IAA in these plants may promote PtoDC3000 growth independent of host auxin signaling, perhaps through a direct effect on the pathogen. In support of this, we found that IAA directly impacted the pathogen, by modulating expression of bacterial virulence genes, both in liquid culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.