Comparative genomics of<i>Pseudomonas syringae</i>pathovar<i>tomato</i>reveals novel chemotaxis pathways associated with motility and plant pathogenicity

Clarke, Christopher R.; Hayes, Byron W.; Runde, Brendan J.; Markel, Eric; Swingle, Bryan; Vinatzer, Boris A.

doi:10.7717/peerj.2570

Cited by 23 publications

(16 citation statements)

References 58 publications

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“…Swimming motility of P. syringae pv. tomato DC3000 wild type (WT) and indicated mutants with empty vector (EV), pJN105 (79), or ϩAlgU expression vector pEM53 (80). Each strain was inoculated on Kings B (KB) medium (77) with 0.3% agar and incubated at 28°C for 24 h.…”

Section: Resultsmentioning

confidence: 99%

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

Bao

Wei

et al. 2020

J Bacteriol

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Flagella power bacterial movement through liquids and over surfaces to access or avoid certain environmental conditions, ultimately increasing a cell’s probability of survival and reproduction. In some cases, flagella and chemotaxis are key virulence factors enabling pathogens to gain entry and attach to suitable host tissues. However, flagella are not always beneficial; both plant and animal immune systems have evolved receptors to sense the proteins that make up flagellar filaments as signatures of bacterial infection. Microbes poorly adapted to avoid or counteract these immune functions are unlikely to be successful in host environments, and this selective pressure has driven the evolution of diverse and often redundant pathogen compensatory mechanisms. We tested the role of AlgU, the Pseudomonas extracytoplasmic function sigma factor σE/σ22 ortholog, in regulating flagellar expression in the context of Pseudomonas syringae-plant interactions. We found that AlgU is necessary for downregulating bacterial flagellin expression in planta and that this results in a corresponding reduction in plant immune elicitation. This AlgU-dependent regulation of flagellin gene expression is beneficial to bacterial growth in the course of plant infection, and eliminating the plant’s ability to detect flagellin makes this AlgU-dependent function irrelevant for bacteria growing in the apoplast. Together, these results add support to an emerging model in which P. syringae AlgU functions at a key control point that serves to optimize the expression of bacterial functions during host interactions, including minimizing the expression of immune elicitors and concomitantly upregulating beneficial virulence functions. IMPORTANCE Foliar plant pathogens, like Pseudomonas syringae, adjust their physiology and behavior to facilitate host colonization and disease, but the full extent of these adaptations is not known. Plant immune systems are triggered by bacterial molecules, such as the proteins that make up flagellar filaments. In this study, we found that during plant infection, AlgU, a gene expression regulator that is responsive to external stimuli, downregulates expression of fliC, which encodes the flagellin protein, a strong elicitor of plant immune systems. This change in gene expression and resultant change in behavior correlate with reduced plant immune activation and improved P. syringae plant colonization. The results of this study demonstrate the proximate and ultimate causes of flagellar regulation in a plant-pathogen interaction.

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Section: Resultsmentioning

confidence: 99%

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

Bao

Wei

et al. 2020

J Bacteriol

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“…Many bacteria use flagella-driven motility to respond to changes in their chemical environment, a process known as chemotaxis (Berg and Brown, 1972;Wadhams and Armitage, 2004;Clarke et al, 2016). In P. aeruginosa, chemotaxis pathwayrelated genes play an important role in flagellar motility, T4 pili formation, and biofilm formation (Hickman et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…In P. aeruginosa, chemotaxis pathwayrelated genes play an important role in flagellar motility, T4 pili formation, and biofilm formation (Hickman et al, 2005). In Pseudomonas savastanoi and PstDC3000, chemotaxis plays a role in virulence (Matas et al, 2012;Clarke et al, 2016) and the rsmA2/rsmA3 mutant of PstDC3000 showed significantly reduced motility (Ge et al, 2019). It is well established that CsrA binding of flhD inhibits RNase E-mediated cleavage and enhances its translation rate in E. coli (Wei et al, 2001;Yakhnin et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

The RsmA RNA-Binding Proteins in Pseudomonas syringae Exhibit Distinct and Overlapping Roles in Modulating Virulence and Survival Under Different Nutritional Conditions

et al. 2021

Front. Plant Sci.

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The post-transcriptional regulator RsmA globally controls gene expression in bacteria. Previous studies showed that RsmA2 and RsmA3 played critical roles in regulating type III secretion system (T3SS), motility, syringafactin, and alginate productions in Pseudomonas syringae pv. tomato strain DC3000 (PstDC3000). In this study, we investigated global gene expression profiles of the wild-type PstDC3000, the rsmA3 mutant, and the rsmA2/A3 double mutant in the hrp-inducing minimum medium (HMM) and King’s B (KB) medium. By comparing the rsmA2/A3 and rsmA3 mutants to PstDC3000, a total of 1358 and 1074 differentially expressed genes (DEGs) in HMM, and 870 and 1463 DEGs in KB were uncovered, respectively. When comparing the rsmA2/A3 mutant with the rsmA3 mutant, 277 and 741 DEGs in HMM and KB, respectively, were revealed. Transcriptomic analysis revealed that the rsmY, rsmZ, and rsmX1-5 non-coding small RNAs (ncsRNAs) were positively affected by RsmA2 and RsmA3, while RsmA3 positively regulates the expression of the rsmA2 gene and negatively regulates both rsmA1 and rsmA5 gene expression. Comparative transcriptomic analysis showed that RsmA2 and RsmA3 synergistically influenced the expression of genes involved in T3SS and alginate biosynthesis in HMM and chemotaxis in KB. RsmA2 and RsmA3 inversely affected genes involved in syringafactin production in HMM and ribosomal protein biosynthesis in KB. In addition, RsmA2 played a major role in influencing genes involved in sarcosine and thiamine biosynthesis in HMM and in mannitol and phosphate metabolism in KB. On the other hand, genes involved in fatty acid metabolism, cellulose biosynthesis, signal transduction, and stress responses were mainly impacted by RsmA3 in both HMM and KB; whereas RsmA3 played a major role in controlling genes involved in c-di-GMP, phosphate metabolism, chemotaxis, and capsular polysaccharide in HMM. Furthermore, regulation of syringafactin production and oxidative stress by RsmA2 and RsmA3 was experimentally verified. Our results suggested the potential interplay among the RsmA proteins, which exhibit distinct and overlapping roles in modulating virulence and survival in P. syringae under different nutritional conditions.

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“…Within this group of mutations, we identified two genes present in both DQS4 T and SmR1: cheY (DQS_RS02075 and HSERO_RS09745), which is related to chemotaxis, and ampD (DQS_RS17190 and HSERO_RS01880), which is involved in peptidoglycan degradation. Chemotaxis is directly involved in modulating the movement of the flagellum in response to attractants, helping bacterial orientation and active motion for survival toward favorable conditions (31)(32)(33). In addition, four other genes encoding transmembrane chemoreceptors, also known as methyl-accepting chemotaxis proteins (MCPs), were identified in H. seropedicae.…”

Section: Fig 1 Tnseq Representation and Determination (A)mentioning

confidence: 99%

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

Amaral

Tuleski

Pankievicz

et al. 2020

mBio

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The plant rhizosphere harbors a diverse population of microorganisms, including beneficial plant growth-promoting bacteria (PGPB), that colonize plant roots and enhance growth and productivity. In order to specifically define bacterial traits that contribute to this beneficial interaction, we used high-throughput transposon mutagenesis sequencing (TnSeq) in two model root-bacterium systems associated with Setaria viridis: Azoarcus olearius DQS4T and Herbaspirillum seropedicae SmR1. This approach identified ∼100 significant genes for each bacterium that appeared to confer a competitive advantage for root colonization. Most of the genes identified specifically in A. olearius encoded metabolism functions, whereas genes identified in H. seropedicae were motility related, suggesting that each strain requires unique functions for competitive root colonization. Genes were experimentally validated by site-directed mutagenesis, followed by inoculation of the mutated bacteria onto S. viridis roots individually, as well as in competition with the wild-type strain. The results identify key bacterial functions involved in iron uptake, polyhydroxybutyrate metabolism, and regulation of aromatic metabolism as important for root colonization. The hope is that by improving our understanding of the molecular mechanisms used by PGPB to colonize plants, we can increase the adoption of these bacteria in agriculture to improve the sustainability of modern cropping systems.IMPORTANCE There is growing interest in the use of associative, plant growth-promoting bacteria (PGPB) as biofertilizers to serve as a sustainable alternative for agriculture application. While a variety of mechanisms have been proposed to explain bacterial plant growth promotion, the molecular details of this process remain unclear. The current research supports the idea that PGPB use in agriculture will be promoted by gaining more knowledge as to how these bacteria colonize plants, promote growth, and do so consistently. Specifically, the research seeks to identify those bacterial genes involved in the ability of two, PGPB strains, Azoarcus olearius and Herbaspirillum seropedicae, to colonize the roots of the C4 model grass Setaria viridis. Applying a transposon mutagenesis (TnSeq) approach, we assigned phenotypes and function to genes that affect bacterial competitiveness during root colonization. The results suggest that each bacterial strain requires unique functions for root colonization but also suggests that a few, critical functions are needed by both bacteria, pointing to some common mechanisms. The hope is that such information can be exploited to improve the use and performance of PGPB in agriculture.

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Comparative genomics ofPseudomonas syringaepathovartomatoreveals novel chemotaxis pathways associated with motility and plant pathogenicity

Cited by 23 publications

References 58 publications

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

The RsmA RNA-Binding Proteins in Pseudomonas syringae Exhibit Distinct and Overlapping Roles in Modulating Virulence and Survival Under Different Nutritional Conditions

Diverse Bacterial Genes Modulate Plant Root Association by Beneficial Bacteria

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