Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco

ABSTRACT Plants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum. SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA...

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Autores principales:	Tiffany M. Lowe-Power, Jonathan M. Jacobs, Florent Ailloud, Brianna Fochs, Philippe Prior, Caitilyn Allen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7e368a912a8c4176adc533fb90efa42b
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spelling	oai:doaj.org-article:7e368a912a8c4176adc533fb90efa42b2021-11-15T15:50:15ZDegradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco10.1128/mBio.00656-162150-7511https://doaj.org/article/7e368a912a8c4176adc533fb90efa42b2016-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00656-16https://doaj.org/toc/2150-7511ABSTRACT Plants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum. SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA via gentisic acid to pyruvate and fumarate. R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis. Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses. Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system, suggesting that this pathogen may suppress virulence functions when stressed. A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato. This may be because SA is less important than gentisic acid in tomato defense signaling. However, another host, tobacco, responds strongly to SA. To test the hypothesis that SA degradation contributes to virulence on tobacco, we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60, which lacks SA degradation genes. Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco. Together, these results suggest that R. solanacearum degrades plant SA to protect itself from inhibitory levels of this compound and also to enhance its virulence on plant hosts like tobacco that use SA as a defense signal molecule. IMPORTANCE Plant pathogens such as the bacterial wilt agent Ralstonia solanacearum threaten food and economic security by causing significant losses for small- and large-scale growers of tomato, tobacco, banana, potato, and ornamentals. Like most plants, these crop hosts use salicylic acid (SA) both indirectly as a signal to activate defenses and directly as an antimicrobial chemical. We found that SA inhibits growth of R. solanacearum and induces a general stress response that includes repression of multiple bacterial wilt virulence factors. The ability to degrade SA reduces the pathogen’s sensitivity to SA toxicity and increases its virulence on tobacco.Tiffany M. Lowe-PowerJonathan M. JacobsFlorent AilloudBrianna FochsPhilippe PriorCaitilyn AllenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Tiffany M. Lowe-Power Jonathan M. Jacobs Florent Ailloud Brianna Fochs Philippe Prior Caitilyn Allen Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
description	ABSTRACT Plants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum. SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA via gentisic acid to pyruvate and fumarate. R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis. Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses. Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system, suggesting that this pathogen may suppress virulence functions when stressed. A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato. This may be because SA is less important than gentisic acid in tomato defense signaling. However, another host, tobacco, responds strongly to SA. To test the hypothesis that SA degradation contributes to virulence on tobacco, we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60, which lacks SA degradation genes. Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco. Together, these results suggest that R. solanacearum degrades plant SA to protect itself from inhibitory levels of this compound and also to enhance its virulence on plant hosts like tobacco that use SA as a defense signal molecule. IMPORTANCE Plant pathogens such as the bacterial wilt agent Ralstonia solanacearum threaten food and economic security by causing significant losses for small- and large-scale growers of tomato, tobacco, banana, potato, and ornamentals. Like most plants, these crop hosts use salicylic acid (SA) both indirectly as a signal to activate defenses and directly as an antimicrobial chemical. We found that SA inhibits growth of R. solanacearum and induces a general stress response that includes repression of multiple bacterial wilt virulence factors. The ability to degrade SA reduces the pathogen’s sensitivity to SA toxicity and increases its virulence on tobacco.
format	article
author	Tiffany M. Lowe-Power Jonathan M. Jacobs Florent Ailloud Brianna Fochs Philippe Prior Caitilyn Allen
author_facet	Tiffany M. Lowe-Power Jonathan M. Jacobs Florent Ailloud Brianna Fochs Philippe Prior Caitilyn Allen
author_sort	Tiffany M. Lowe-Power
title	Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
title_short	Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
title_full	Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
title_fullStr	Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
title_full_unstemmed	Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco
title_sort	degradation of the plant defense signal salicylic acid protects <named-content content-type="genus-species">ralstonia solanacearum</named-content> from toxicity and enhances virulence on tobacco
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/7e368a912a8c4176adc533fb90efa42b
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Degradation of the Plant Defense Signal Salicylic Acid Protects <named-content content-type="genus-species">Ralstonia solanacearum</named-content> from Toxicity and Enhances Virulence on Tobacco

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