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1. Dual Role of Auxin in Regulating Plant Defense and Bacterial Virulence Gene Expression During Pseudomonas syringae PtoDC3000 Pathogenesis

   https://doi.org/10.1094/MPMI-02-20-0047-R  

   Djami-Tchatchou, Arnaud T.; Harrison, Gregory A.; Harper, Chris P.; Wang, Renhou; Prigge, Michael J.; Estelle, Mark; Kunkel, Barbara N. (August 2020, Molecular Plant-Microbe Interactions®)

   null (Ed.)

   Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen strain Pseudomonas syringae DC3000 (PtoDC3000) produces the plant hormone auxin (indole-3-acetic acid [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 and that this phenotype was suppressed by introducing the sid2-2 mutation, which impairs SA synthesis. Thus, host auxin signaling is required for normal susceptibility to PtoDC3000 and is involved in suppressing SA-mediated defenses. Unexpectedly, tir1 afb1 afb4 afb5 quadruple-mutant plants lacking four of the six known auxin coreceptors that exhibit decreased auxin perception, supported increased levels of bacterial growth. This mutant exhibited elevated IAA levels and reduced SA-mediated defenses, providing additional evidence that auxin promotes disease by suppressing host defense. We also investigated the hypothesis that IAA promotes PtoDC3000 virulence through a direct effect on the pathogen and found that IAA modulates expression of virulence genes, both in culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression. 

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2. Occurrence, Function, and Biosynthesis of the Natural Auxin Phenylacetic Acid (PAA) in Plants

   https://doi.org/10.3390/plants12020266  

   Perez, Veronica C.; Zhao, Haohao; Lin, Makou; Kim, Jeongim (January 2023, Plants)

   Auxins are a class of plant hormones playing crucial roles in a plant’s growth, development, and stress responses. Phenylacetic acid (PAA) is a phenylalanine-derived natural auxin found widely in plants. Although the auxin activity of PAA in plants was identified several decades ago, PAA homeostasis and its function remain poorly understood, whereas indole-3-acetic acid (IAA), the most potent auxin, has been used for most auxin studies. Recent studies have revealed unique features of PAA distinctive from IAA, and the enzymes and intermediates of the PAA biosynthesis pathway have been identified. Here, we summarize the occurrence and function of PAA in plants and highlight the recent progress made in PAA homeostasis, emphasizing PAA biosynthesis and crosstalk between IAA and PAA homeostasis. 

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3. Investigating the reaction and substrate preference of indole-3-acetaldehyde dehydrogenase from the plant pathogen Pseudomonas syringae Pto DC3000

   https://doi.org/10.1042/BSR20202959  

   Zhang, Kaleena; Lee, Josephine S.; Liu, Regina; Chan, Zita T.; Dawson, Trenton J.; De Togni, Elisa S.; Edwards, Chris T.; Eng, Isabel K.; Gao, Ashley R.; Goicouria, Luis A.; et al (December 2020, Bioscience Reports)

   null (Ed.)

   Abstract Aldehyde dehydrogenases (ALDHs) catalyze the conversion of various aliphatic and aromatic aldehydes into corresponding carboxylic acids. Traditionally considered as housekeeping enzymes, new biochemical roles are being identified for members of ALDH family. Recent work showed that AldA from the plant pathogen Pseudomonas syringae strain PtoDC3000 (PtoDC3000) functions as an indole-3-acetaldehyde dehydrogenase for the synthesis of indole-3-acetic acid (IAA). IAA produced by AldA allows the pathogen to suppress salicylic acid-mediated defenses in the model plant Arabidopsis thaliana. Here we present a biochemical and structural analysis of the AldA indole-3-acetaldehyde dehydrogenase from PtoDC3000. Site-directed mutants targeting the catalytic residues Cys302 and Glu267 resulted in a loss of enzymatic activity. The X-ray crystal structure of the catalytically inactive AldA C302A mutant in complex with IAA and NAD+ showed the cofactor adopting a conformation that differs from the previously reported structure of AldA. These structures suggest that NAD+ undergoes a conformational change during the AldA reaction mechanism similar to that reported for human ALDH. Site-directed mutagenesis of the IAA binding site indicates that changes in the active site surface reduces AldA activity; however, substitution of Phe169 with a tryptophan altered the substrate selectivity of the mutant to prefer octanal. The present study highlights the inherent biochemical versatility of members of the ALDH enzyme superfamily in P. syringae. 

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4. Auxin Plays Multiple Roles during Plant–Pathogen Interactions

   https://doi.org/10.1101/cshperspect.a040022  

   Kunkel, Barbara N.; Johnson, Joshua M.B. (January 2021, Cold Spring Harbor Perspectives in Biology)

   Weijers, D.; Ljung, K.; Estelle, M.; Leyser, O. (Ed.)

   The plant hormone auxin governs many aspects of normal plant growth and development. Auxin also plays an important role in plant–microbe interactions, including interactions between plant hosts and pathogenic microorganisms that cause disease. It is now well established that indole-3-acetic acid (IAA), the most well-studied form of auxin, promotes disease in many plant–pathogen interactions. Recent studies have shown that IAA can act both as a plant hormone that modulates host signaling and physiology to increase host susceptibility and as a microbial signal that directly impacts the pathogen to promote virulence, but large gaps in our understanding remain. In this article, we review recent studies on the roles that auxin plays during plant–pathogen interactions and discuss the virulence mechanisms that many plant pathogens have evolved to manipulate host auxin signaling and promote pathogenesis. 

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5. Diverse MarR bacterial regulators of auxin catabolism in the plant microbiome

   https://doi.org/10.1038/s41564-022-01244-3  

   Conway, Jonathan M.; Walton, William G.; Salas-González, Isai; Law, Theresa F.; Lindberg, Chloe A.; Crook, Laura E.; Kosina, Suzanne M.; Fitzpatrick, Connor R.; Lietzan, Adam D.; Northen, Trent R.; et al (October 2022, Nature Microbiology)

   Abstract Chemical signalling in the plant microbiome can have drastic effects on microbial community structure, and on host growth and development. Previously, we demonstrated that the auxin metabolic signal interference performed by the bacterial genusVariovoraxvia an auxin degradation locus was essential for maintaining stereotypic root development in an ecologically relevant bacterial synthetic community. Here, we dissect theVariovoraxauxin degradation locus to define the genesiadDEas necessary and sufficient for indole-3-acetic acid (IAA) degradation and signal interference. We determine the crystal structures and binding properties of the operon’s MarR-family repressor with IAA and other auxins. Auxin degradation operons were identified across the bacterial tree of life and we define two distinct types on the basis of gene content and metabolic products:iac-like andiad-like. The structures of MarRs from representatives of each auxin degradation operon type establish that each has distinct IAA-binding pockets. Comparison of representative IAA-degrading strains from diverse bacterial genera colonizingArabidopsisplants show that while all degrade IAA, only strains containingiad-like auxin-degrading operons interfere with auxin signalling in a complex synthetic community context. This suggests thatiad-like operon-containing bacterial strains, includingVariovoraxspecies, play a key ecological role in modulating auxins in the plant microbiome. 

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