A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate

ABSTRACT  The plant pathogen Ralstonia solanacearum possesses two genes encoding a trehalose-6-phosphate synthase (TPS), an enzyme of the trehalose biosynthetic pathway. One of these genes, named ripTPS, was found to encode a protein with an additional N-terminal domain which directs its translocati...

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Autores principales: M. Poueymiro, A. C. Cazalé, J. M. François, J. L. Parrou, N. Peeters, S. Genin
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:9beaee7fb25f4baaa3bdfc94186832332021-11-15T15:47:04ZA <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate10.1128/mBio.02065-142150-7511https://doaj.org/article/9beaee7fb25f4baaa3bdfc94186832332014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02065-14https://doaj.org/toc/2150-7511ABSTRACT  The plant pathogen Ralstonia solanacearum possesses two genes encoding a trehalose-6-phosphate synthase (TPS), an enzyme of the trehalose biosynthetic pathway. One of these genes, named ripTPS, was found to encode a protein with an additional N-terminal domain which directs its translocation into host plant cells through the type 3 secretion system. RipTPS is a conserved effector in the R. solanacearum species complex, and homologues were also detected in other bacterial plant pathogens. Functional analysis of RipTPS demonstrated that this type 3 effector synthesizes trehalose-6-phosphate and identified residues essential for this enzymatic activity. Although trehalose-6-phosphate is a key signal molecule in plants that regulates sugar status and carbon assimilation, the disruption of ripTPS did not alter the virulence of R. solanacearum on plants. However, heterologous expression assays showed that this effector specifically elicits a hypersensitive-like response on tobacco that is independent of its enzymatic activity and is triggered by the C-terminal half of the protein. Recognition of this effector by the plant immune system is suggestive of a role during the infectious process. IMPORTANCE Ralstonia solanacearum, the causal agent of bacterial wilt disease, infects more than two hundred plant species, including economically important crops. The type III secretion system plays a major role in the pathogenicity of this bacterium, and approximately 70 effector proteins have been shown to be translocated into host plant cells. This study provides the first description of a type III effector endowed with a trehalose-6-phosphate synthase enzymatic activity and illustrates a new mechanism by which the bacteria may manipulate the plant metabolism upon infection. In recent years, trehalose-6-phosphate has emerged as an essential signal molecule in plants, connecting plant metabolism and development. The finding that a bacterial pathogen could induce the production of trehalose-6-phosphate in plant cells further highlights the importance of this metabolite in multiple aspects of the molecular physiology of plants.M. PoueymiroA. C. CazaléJ. M. FrançoisJ. L. ParrouN. PeetersS. GeninAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
M. Poueymiro
A. C. Cazalé
J. M. François
J. L. Parrou
N. Peeters
S. Genin
A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
description ABSTRACT  The plant pathogen Ralstonia solanacearum possesses two genes encoding a trehalose-6-phosphate synthase (TPS), an enzyme of the trehalose biosynthetic pathway. One of these genes, named ripTPS, was found to encode a protein with an additional N-terminal domain which directs its translocation into host plant cells through the type 3 secretion system. RipTPS is a conserved effector in the R. solanacearum species complex, and homologues were also detected in other bacterial plant pathogens. Functional analysis of RipTPS demonstrated that this type 3 effector synthesizes trehalose-6-phosphate and identified residues essential for this enzymatic activity. Although trehalose-6-phosphate is a key signal molecule in plants that regulates sugar status and carbon assimilation, the disruption of ripTPS did not alter the virulence of R. solanacearum on plants. However, heterologous expression assays showed that this effector specifically elicits a hypersensitive-like response on tobacco that is independent of its enzymatic activity and is triggered by the C-terminal half of the protein. Recognition of this effector by the plant immune system is suggestive of a role during the infectious process. IMPORTANCE Ralstonia solanacearum, the causal agent of bacterial wilt disease, infects more than two hundred plant species, including economically important crops. The type III secretion system plays a major role in the pathogenicity of this bacterium, and approximately 70 effector proteins have been shown to be translocated into host plant cells. This study provides the first description of a type III effector endowed with a trehalose-6-phosphate synthase enzymatic activity and illustrates a new mechanism by which the bacteria may manipulate the plant metabolism upon infection. In recent years, trehalose-6-phosphate has emerged as an essential signal molecule in plants, connecting plant metabolism and development. The finding that a bacterial pathogen could induce the production of trehalose-6-phosphate in plant cells further highlights the importance of this metabolite in multiple aspects of the molecular physiology of plants.
format article
author M. Poueymiro
A. C. Cazalé
J. M. François
J. L. Parrou
N. Peeters
S. Genin
author_facet M. Poueymiro
A. C. Cazalé
J. M. François
J. L. Parrou
N. Peeters
S. Genin
author_sort M. Poueymiro
title A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
title_short A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
title_full A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
title_fullStr A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
title_full_unstemmed A <named-content content-type="genus-species">Ralstonia solanacearum</named-content> Type III Effector Directs the Production of the Plant Signal Metabolite Trehalose-6-Phosphate
title_sort <named-content content-type="genus-species">ralstonia solanacearum</named-content> type iii effector directs the production of the plant signal metabolite trehalose-6-phosphate
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/9beaee7fb25f4baaa3bdfc9418683233
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