The biotroph Agrobacterium tumefaciens thrives in tumors by exploiting a wide spectrum of plant host metabolites.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
04 2019
Historique:
received: 22 08 2018
accepted: 03 11 2018
pubmed: 18 11 2018
medline: 28 2 2020
entrez: 18 11 2018
Statut: ppublish

Résumé

Agrobacterium tumefaciens is a niche-constructing biotroph that exploits host plant metabolites. We combined metabolomics, transposon-sequencing (Tn-seq), transcriptomics, and reverse genetics to characterize A. tumefaciens pathways involved in the exploitation of resources from the Solanum lycopersicum host plant. Metabolomics of healthy stems and plant tumors revealed the common (e.g. sucrose, glutamate) and enriched (e.g. opines, γ-aminobutyric acid (GABA), γ-hydroxybutyric acid (GHB), pyruvate) metabolites that A. tumefaciens could use as nutrients. Tn-seq and transcriptomics pinpointed the genes that are crucial and/or upregulated when the pathogen grew on either sucrose (pgi, kdgA, pycA, cisY) or GHB (blcAB, pckA, eno, gpsA) as a carbon source. While sucrose assimilation involved the Entner-Doudoroff and tricarboxylic acid (TCA) pathways, GHB degradation required the blc genes, TCA cycle, and gluconeogenesis. The tumor-enriched metabolite pyruvate is at the node connecting these pathways. Using reverse genetics, we showed that the blc, pckA, and pycA loci were important for aggressiveness (tumor weight), proliferation (bacterial charge), and/or fitness (competition between the constructed mutants and wild-type) of A. tumefaciens in plant tumors. This work highlighted how a biotroph mobilizes its central metabolism for exploiting a wide diversity of resources in a plant host. It further shows the complementarity of functional genome-wide scans by transcriptomics and Tn-seq to decipher the lifestyle of a plant pathogen.

Identifiants

pubmed: 30447163
doi: 10.1111/nph.15598
doi:

Substances chimiques

DNA Transposable Elements 0
Hydroxybutyrates 0
4-hydroxybutyric acid 30IW36W5B2
gamma-Aminobutyric Acid 56-12-2
Sucrose 57-50-1
Carbon 7440-44-0
Nitrogen N762921K75

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

455-467

Subventions

Organisme : Université Paris-Saclay
ID : PhD2014-2016
Pays : International
Organisme : Centre National de la Recherche Scientifique
ID : SE2016-2017
Pays : International
Organisme : LabEx Saclay Plant Sciences-SPS
ID : ANR-10-LABX-0040-SPS
Pays : International

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.

Auteurs

Almudena Gonzalez-Mula (A)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Joy Lachat (J)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Léo Mathias (L)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Delphine Naquin (D)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Florian Lamouche (F)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Peter Mergaert (P)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

Denis Faure (D)

Institute for Integrative Biology of the Cell (I2BC), CNRS CEA University Paris-Sud, University Paris-Saclay, Gif-sur-Yvette, F-91190, France.

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Classifications MeSH