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Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants

Pseudomonas aeruginosa strain PA14 is a multi-host pathogen that infects plants, nematodes, insects, and vertebrates. Many PA14 factors are required for virulence in more than one of these hosts. Noting that plants have a fundamentally different cellular architecture from animals, we sought to ident...

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Autores principales: Djonović, Slavica, Urbach, Jonathan M., Drenkard, Eliana, Bush, Jenifer, Feinbaum, Rhonda, Ausubel, Jonathan L., Traficante, David, Risech, Martina, Kocks, Christine, Fischbach, Michael A., Priebe, Gregory P., Ausubel, Frederick M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3591346/
https://www.ncbi.nlm.nih.gov/pubmed/23505373
http://dx.doi.org/10.1371/journal.ppat.1003217
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author Djonović, Slavica
Urbach, Jonathan M.
Drenkard, Eliana
Bush, Jenifer
Feinbaum, Rhonda
Ausubel, Jonathan L.
Traficante, David
Risech, Martina
Kocks, Christine
Fischbach, Michael A.
Priebe, Gregory P.
Ausubel, Frederick M.
author_facet Djonović, Slavica
Urbach, Jonathan M.
Drenkard, Eliana
Bush, Jenifer
Feinbaum, Rhonda
Ausubel, Jonathan L.
Traficante, David
Risech, Martina
Kocks, Christine
Fischbach, Michael A.
Priebe, Gregory P.
Ausubel, Frederick M.
author_sort Djonović, Slavica
collection PubMed
description Pseudomonas aeruginosa strain PA14 is a multi-host pathogen that infects plants, nematodes, insects, and vertebrates. Many PA14 factors are required for virulence in more than one of these hosts. Noting that plants have a fundamentally different cellular architecture from animals, we sought to identify PA14 factors that are specifically required for plant pathogenesis. We show that synthesis by PA14 of the disaccharide trehalose is required for pathogenesis in Arabidopsis, but not in nematodes, insects, or mice. In-frame deletion of two closely-linked predicted trehalose biosynthetic operons, treYZ and treS, decreased growth in Arabidopsis leaves about 50 fold. Exogenously co-inoculated trehalose, ammonium, or nitrate, but not glucose, sulfate, or phosphate suppressed the phenotype of the double ΔtreYZΔtreS mutant. Exogenous trehalose or ammonium nitrate does not suppress the growth defect of the double ΔtreYZΔtreS mutant by suppressing the plant defense response. Trehalose also does not function intracellularly in P. aeruginosa to ameliorate a variety of stresses, but most likely functions extracellularly, because wild-type PA14 rescued the in vivo growth defect of the ΔtreYZΔtreS in trans. Surprisingly, the growth defect of the double ΔtreYZΔtreS double mutant was suppressed by various Arabidopsis cell wall mutants that affect xyloglucan synthesis, including an xxt1xxt2 double mutant that completely lacks xyloglucan, even though xyloglucan mutants are not more susceptible to pathogens and respond like wild-type plants to immune elicitors. An explanation of our data is that trehalose functions to promote the acquisition of nitrogen-containing nutrients in a process that involves the xyloglucan component of the plant cell wall, thereby allowing P. aeruginosa to replicate in the intercellular spaces in a leaf. This work shows how P. aeruginosa, a multi-host opportunistic pathogen, has repurposed a highly conserved “house-keeping” anabolic pathway (trehalose biosynthesis) as a potent virulence factor that allows it to replicate in the intercellular environment of a leaf.
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spelling pubmed-35913462013-03-15 Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants Djonović, Slavica Urbach, Jonathan M. Drenkard, Eliana Bush, Jenifer Feinbaum, Rhonda Ausubel, Jonathan L. Traficante, David Risech, Martina Kocks, Christine Fischbach, Michael A. Priebe, Gregory P. Ausubel, Frederick M. PLoS Pathog Research Article Pseudomonas aeruginosa strain PA14 is a multi-host pathogen that infects plants, nematodes, insects, and vertebrates. Many PA14 factors are required for virulence in more than one of these hosts. Noting that plants have a fundamentally different cellular architecture from animals, we sought to identify PA14 factors that are specifically required for plant pathogenesis. We show that synthesis by PA14 of the disaccharide trehalose is required for pathogenesis in Arabidopsis, but not in nematodes, insects, or mice. In-frame deletion of two closely-linked predicted trehalose biosynthetic operons, treYZ and treS, decreased growth in Arabidopsis leaves about 50 fold. Exogenously co-inoculated trehalose, ammonium, or nitrate, but not glucose, sulfate, or phosphate suppressed the phenotype of the double ΔtreYZΔtreS mutant. Exogenous trehalose or ammonium nitrate does not suppress the growth defect of the double ΔtreYZΔtreS mutant by suppressing the plant defense response. Trehalose also does not function intracellularly in P. aeruginosa to ameliorate a variety of stresses, but most likely functions extracellularly, because wild-type PA14 rescued the in vivo growth defect of the ΔtreYZΔtreS in trans. Surprisingly, the growth defect of the double ΔtreYZΔtreS double mutant was suppressed by various Arabidopsis cell wall mutants that affect xyloglucan synthesis, including an xxt1xxt2 double mutant that completely lacks xyloglucan, even though xyloglucan mutants are not more susceptible to pathogens and respond like wild-type plants to immune elicitors. An explanation of our data is that trehalose functions to promote the acquisition of nitrogen-containing nutrients in a process that involves the xyloglucan component of the plant cell wall, thereby allowing P. aeruginosa to replicate in the intercellular spaces in a leaf. This work shows how P. aeruginosa, a multi-host opportunistic pathogen, has repurposed a highly conserved “house-keeping” anabolic pathway (trehalose biosynthesis) as a potent virulence factor that allows it to replicate in the intercellular environment of a leaf. Public Library of Science 2013-03-07 /pmc/articles/PMC3591346/ /pubmed/23505373 http://dx.doi.org/10.1371/journal.ppat.1003217 Text en © 2013 Djonović et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Djonović, Slavica
Urbach, Jonathan M.
Drenkard, Eliana
Bush, Jenifer
Feinbaum, Rhonda
Ausubel, Jonathan L.
Traficante, David
Risech, Martina
Kocks, Christine
Fischbach, Michael A.
Priebe, Gregory P.
Ausubel, Frederick M.
Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title_full Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title_fullStr Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title_full_unstemmed Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title_short Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants
title_sort trehalose biosynthesis promotes pseudomonas aeruginosa pathogenicity in plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3591346/
https://www.ncbi.nlm.nih.gov/pubmed/23505373
http://dx.doi.org/10.1371/journal.ppat.1003217
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