Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization

ABSTRACT The plant pathogen Pseudomonas syringae pv. syringae B728a grows and survives on leaf surfaces and in the leaf apoplast of its host, bean (Phaseolus vulgaris). To understand the contribution of distinct regulators to B728a fitness and pathogenicity, we performed a transcriptome analysis of...

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Autores principales:	Xilan Yu, Steven P. Lund, Jessica W. Greenwald, Angela H. Records, Russell A. Scott, Dan Nettleton, Steven E. Lindow, Dennis C. Gross, Gwyn A. Beattie
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4bc1f9efbe8a463ebcf1c3e92fb45971
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spelling	oai:doaj.org-article:4bc1f9efbe8a463ebcf1c3e92fb459712021-11-15T15:45:54ZTranscriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization10.1128/mBio.01683-142150-7511https://doaj.org/article/4bc1f9efbe8a463ebcf1c3e92fb459712014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01683-14https://doaj.org/toc/2150-7511ABSTRACT The plant pathogen Pseudomonas syringae pv. syringae B728a grows and survives on leaf surfaces and in the leaf apoplast of its host, bean (Phaseolus vulgaris). To understand the contribution of distinct regulators to B728a fitness and pathogenicity, we performed a transcriptome analysis of strain B728a and nine regulatory mutants recovered from the surfaces and interior of leaves and exposed to environmental stresses in culture. The quorum-sensing regulators AhlR and AefR influenced few genes in planta or in vitro. In contrast, GacS and a downstream regulator, SalA, formed a large regulatory network that included a branch that regulated diverse traits and was independent of plant-specific environmental signals and a plant signal-dependent branch that positively regulated secondary metabolite genes and negatively regulated the type III secretion system. SalA functioned as a central regulator of iron status based on its reciprocal regulation of pyoverdine and achromobactin genes and also sulfur uptake, suggesting a role in the iron-sulfur balance. RetS functioned almost exclusively to repress secondary metabolite genes when the cells were not on leaves. Among the sigma factors examined, AlgU influenced many more genes than RpoS, and most AlgU-regulated genes depended on RpoN. RpoN differentially impacted many AlgU- and GacS-activated genes in cells recovered from apoplastic versus epiphytic sites, suggesting differences in environmental signals or bacterial stress status in these two habitats. Collectively, our findings illustrate a central role for GacS, SalA, RpoN, and AlgU in global regulation in B728a in planta and a high level of plasticity in these regulators’ responses to distinct environmental signals. IMPORTANCE Leaves harbor abundant microorganisms, all of which must withstand challenges such as active plant defenses and a highly dynamic environment. Some of these microbes can influence plant health. Despite knowledge of individual regulators that affect the fitness or pathogenicity of foliar pathogens, our understanding of the relative importance of various global regulators to leaf colonization is limited. Pseudomonas syringae strain B728a is a plant pathogen and a good colonist of both the surfaces and interior of leaves. This study used global transcript profiles of strain B728a to investigate the complex regulatory network of putative quorum-sensing regulators, two-component regulators, and sigma factors in cells colonizing the leaf surface and leaf interior under stressful in vitro conditions. The results highlighted the value of evaluating these networks in planta due to the impact of leaf-specific environmental signals and suggested signal differences that may enable cells to differentiate surface versus interior leaf habitats.Xilan YuSteven P. LundJessica W. GreenwaldAngela H. RecordsRussell A. ScottDan NettletonSteven E. LindowDennis C. GrossGwyn A. BeattieAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Xilan Yu Steven P. Lund Jessica W. Greenwald Angela H. Records Russell A. Scott Dan Nettleton Steven E. Lindow Dennis C. Gross Gwyn A. Beattie Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
description	ABSTRACT The plant pathogen Pseudomonas syringae pv. syringae B728a grows and survives on leaf surfaces and in the leaf apoplast of its host, bean (Phaseolus vulgaris). To understand the contribution of distinct regulators to B728a fitness and pathogenicity, we performed a transcriptome analysis of strain B728a and nine regulatory mutants recovered from the surfaces and interior of leaves and exposed to environmental stresses in culture. The quorum-sensing regulators AhlR and AefR influenced few genes in planta or in vitro. In contrast, GacS and a downstream regulator, SalA, formed a large regulatory network that included a branch that regulated diverse traits and was independent of plant-specific environmental signals and a plant signal-dependent branch that positively regulated secondary metabolite genes and negatively regulated the type III secretion system. SalA functioned as a central regulator of iron status based on its reciprocal regulation of pyoverdine and achromobactin genes and also sulfur uptake, suggesting a role in the iron-sulfur balance. RetS functioned almost exclusively to repress secondary metabolite genes when the cells were not on leaves. Among the sigma factors examined, AlgU influenced many more genes than RpoS, and most AlgU-regulated genes depended on RpoN. RpoN differentially impacted many AlgU- and GacS-activated genes in cells recovered from apoplastic versus epiphytic sites, suggesting differences in environmental signals or bacterial stress status in these two habitats. Collectively, our findings illustrate a central role for GacS, SalA, RpoN, and AlgU in global regulation in B728a in planta and a high level of plasticity in these regulators’ responses to distinct environmental signals. IMPORTANCE Leaves harbor abundant microorganisms, all of which must withstand challenges such as active plant defenses and a highly dynamic environment. Some of these microbes can influence plant health. Despite knowledge of individual regulators that affect the fitness or pathogenicity of foliar pathogens, our understanding of the relative importance of various global regulators to leaf colonization is limited. Pseudomonas syringae strain B728a is a plant pathogen and a good colonist of both the surfaces and interior of leaves. This study used global transcript profiles of strain B728a to investigate the complex regulatory network of putative quorum-sensing regulators, two-component regulators, and sigma factors in cells colonizing the leaf surface and leaf interior under stressful in vitro conditions. The results highlighted the value of evaluating these networks in planta due to the impact of leaf-specific environmental signals and suggested signal differences that may enable cells to differentiate surface versus interior leaf habitats.
format	article
author	Xilan Yu Steven P. Lund Jessica W. Greenwald Angela H. Records Russell A. Scott Dan Nettleton Steven E. Lindow Dennis C. Gross Gwyn A. Beattie
author_facet	Xilan Yu Steven P. Lund Jessica W. Greenwald Angela H. Records Russell A. Scott Dan Nettleton Steven E. Lindow Dennis C. Gross Gwyn A. Beattie
author_sort	Xilan Yu
title	Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
title_short	Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
title_full	Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
title_fullStr	Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
title_full_unstemmed	Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization
title_sort	transcriptional analysis of the global regulatory networks active in <named-content content-type="genus-species">pseudomonas syringae</named-content> during leaf colonization
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/4bc1f9efbe8a463ebcf1c3e92fb45971
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Transcriptional Analysis of the Global Regulatory Networks Active in <named-content content-type="genus-species">Pseudomonas syringae</named-content> during Leaf Colonization

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