New insights into the role of indole-3-acetic acid in the virulence of<i>Pseudomonas savastanoi</i>pv.<i>savastanoi</i>

Aragón, Isabel M.; Pérez‐Martínez, Isabel; Moreno-Pérez, Alba; Cerezo, Miguel; Ramos, Cayo

doi:10.1111/1574-6968.12413

Cited by 58 publications

(71 citation statements)

References 37 publications

(68 reference statements)

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“…In particular, high IAA concentrations (up to 1 mM) have been found to have a strong inhibitory effect on the TTSS functionality of P. savastanoi pv. savastanoi [29] and further demonstrated herein for P. savastanoi pv. nerii Psn23.…”

Section: Discussionsupporting

confidence: 82%

“…This feature was initially incorrectly believed to be restricted to gall-producing bacteria such as Pseudomonas savastanoi and Pantoea agglomerans, in which IAA secretion was considered to be the main factor directly supporting the development of the hyperplastic symptoms on the host [27,28]. However, it soon became evident that a broader distribution of IAA biosynthesis was also present in several non-gall-inducing phytopathogenic bacteria such as Dickeya dadantii [29]. The best characterized Trp-dependent pathway in bacteria is the two-step process denoted as the indole-3-acetamide (IAM) pathway, where the enzymes tryptophan-2-monooxygenase (IaaM) and IAM hydrolase (IaaH) are encoded by the iaaM and iaaH genes, respectively, and sequentially convert Trp to IAM and then to IAA.…”

Section: Introductionmentioning

confidence: 99%

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Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

Cerboneschi

Decorosi

Biancalani

et al. 2016

Research in Microbiology

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The plant pathogenic bacterium Pseudomonas savastanoi, the causal agent of olive and oleander knot disease, uses the so-called "indole-3-acetamide pathway" to convert tryptophan to indole-3-acetic acid (IAA) via a two-step pathway catalyzed by enzymes encoded by the genes in the iaaM/iaaH operon. Moreover, pathovar nerii of P. savastanoi is able to conjugate IAA to lysine to generate the less biologically active compound IAA-Lys via the enzyme IAA-lysine synthase encoded by the iaaL gene. Interestingly, iaaL is now known to be widespread in many Pseudomonas syringae pathovars, even in the absence of the iaaM and iaaH genes for IAA biosynthesis.Here, two knockout mutants, DiaaL and DiaaM, of strain Psn23 of P. savastanoi pv. nerii were produced. Pathogenicity tests using the host plant Nerium oleander showed that DiaaL and DiaaM were hypervirulent and hypovirulent, respectively and these features appeared to be related to their differential production of free IAA. Using the Phenotype Microarray approach, the chemical sensitivity of these mutants was shown to be comparable to that of wild-type Psn23. The main exception was 8 hydroxyquinoline, a toxic compound that is naturally present in plant exudates and is used as a biocide, which severely impaired the growth of DiaaL and DiaaM, as well as growth of the non-pathogenic mutant DhrpA, which lacks a functional Type Three Secretion System (TTSS). According to bioinformatics analysis of the Psn23 genome, a gene encoding a putative Multidrug and Toxic compound Extrusion (MATE) transporter, was found upstream of iaaL. Similarly to iaaL and iaaM, its expression appeared to be TTSS-dependent. Moreover, auxin-responsive elements were identified for the first time in the modular promoters of both the iaaL gene and the iaaM/iaaH operon of P. savastanoi, suggesting their IAA-inducible transcription. Gene expression analysis of several genes related to TTSS, IAA metabolism and drug resistance confirmed the presence of a concerted regulatory network in this phytopathogen among virulence, fitness and drug efflux.

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Section: Discussionsupporting

confidence: 82%

Section: Introductionmentioning

confidence: 99%

Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

Cerboneschi

Decorosi

Biancalani

et al. 2016

Research in Microbiology

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“…Construction of the single iaaMH1 and the double iaaMH1 iaaMH2 mutants mentioned above in Psv NCPPB 3335 provided direct evidences for the involvement of this operon in Psv pathogenicity. As expected from their low IAA levels, knot induction by these two mutant strains was fully abolished, further supporting the role of IAA as a pathogenicity determinant in this bacterial pathogen (Aragón et al, 2014) ( Figure 2 ).…”

Section: Pathogen-produced Phytohormones and Their Role In Diseasesupporting

confidence: 78%

“…In the model Psv strain NCPPB 3335, the iaaM2 gene encodes an internal insertion of 22 nucleotides. In addition, a knock-out iaaMH2 mutant of this strain produces similar amounts of IAA as the wild-type strain, suggesting that this extra copy of the operon is not functional (Aragón et al, 2014). Interestingly, single- ( iaaMH1 ) and double- ( iaaMH1 and iaaMH2 ) deletion mutants of Psv NCPPB 3335 produce residual amounts of IAA, suggesting that redundancy in the IAA biosynthetic pathways also occurs in P. savastanoi (Aragón et al, 2014).…”

Section: Pathogen-produced Phytohormones and Their Role In Diseasementioning

confidence: 99%

Knots Untie: Molecular Determinants Involved in Knot Formation Induced by Pseudomonas savastanoi in Woody Hosts

et al. 2017

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The study of the molecular basis of tree diseases is lately receiving a renewed attention, especially with the emerging perception that pathogens require specific pathogenicity and virulence factors to successfully colonize woody hosts. Pathosystems involving woody plants are notoriously difficult to study, although the use of model bacterial strains together with genetically homogeneous micropropagated plant material is providing a significant impetus to our understanding of the molecular determinants leading to disease. The gammaproteobacterium Pseudomonas savastanoi belongs to the intensively studied Pseudomonas syringae complex, and includes three pathogenic lineages causing tumorous overgrowths (knots) in diverse economically relevant trees and shrubs. As it occurs with many other bacteria, pathogenicity of P. savastanoi is dependent on a type III secretion system, which is accompanied by a core set of at least 20 effector genes shared among strains isolated from olive, oleander, and ash. The induction of knots of wild-type size requires that the pathogen maintains adequate levels of diverse metabolites, including the phytohormones indole-3-acetic acid and cytokinins, as well as cyclic-di-GMP, some of which can also regulate the expression of other pathogenicity and virulence genes and participate in bacterial competitiveness. In a remarkable example of social networking, quorum sensing molecules allow for the communication among P. savastanoi and other members of the knot microbiome, while at the same time are essential for tumor formation. Additionally, a distinguishing feature of bacteria from the P. syringae complex isolated from woody organs is the possession of a 15 kb genomic island (WHOP) carrying four operons and three other genes involved in degradation of phenolic compounds. Two of these operons mediate the catabolism of anthranilate and catechol and, together with another operon, are required for the induction of full-size tumors in woody hosts, but not in non-woody micropropagated plants. The use of transposon mutagenesis also uncovered a treasure trove of additional P. savastanoi genes affecting virulence and participating in diverse bacterial processes. Although there is still much to be learned on what makes a bacterium a successful pathogen of trees, we are already untying the knots.

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“…Gall-forming bacterial species harbor a horizontally transferred gene cluster that controls auxin biosynthesis via the IAM pathway. Mutants of Pseudomonas savastanoi, the causal agent of olive and oleander knot, which lack this operon, show reduced auxin biosynthesis and attenuated knot symptoms on olive plants (Aragón et al, 2014). Pantoea agglomerans (previously known as Erwinia herbicola) pv gypsophilae harbors machinery to produce auxins via both the IAM and indole-3-pyruvate (IpyA) pathways.…”

Section: Effectors Targeting Auxin Biosynthesis or Signalingmentioning

confidence: 99%

Intervention of Phytohormone Pathways by Pathogen Effectors

2014

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New insights into the role of indole-3-acetic acid in the virulence ofPseudomonas savastanoipv.savastanoi

Cited by 58 publications

References 37 publications

Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

Knots Untie: Molecular Determinants Involved in Knot Formation Induced by Pseudomonas savastanoi in Woody Hosts

Intervention of Phytohormone Pathways by Pathogen Effectors

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