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Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae.

ABSTRACT: The posttranscriptional regulator RsmA controls the production of plant cell wall degrading enzymes (PCWDE) and cell motility in the Pectobacterium genus of plant pathogens. In this study the physiological role of gene regulation by RsmA is under investigation. Disruption of rsmA gene of the Pectobacterium wasabiae strain, SCC3193 resulted in 3-fold decrease in growth rate and increased virulence. The comparison of mRNA levels of the rsmA(-) mutant and wild-type using a genome-wide microarray showed, that genes responsible for successful infection, i.e. virulence factors, motility, butanediol fermentation, various secretion systems etc. were up-regulated in the rsmA(-) strain. The rsmA(-) strain exhibited a higher propensity to swarm and produce PCWDE compared to the wild-type strain. Virulence experiments in potato tubers demonstrated that in spite of its more efficient tissue maceration, the rsmA(-) strain's ability to survive within the host is reduced and the infection site is taken over by resident bacteria. Taken together, in the absence of RsmA, cells revert to a constitutively infective phenotype characterized by expression of virulence factors and swarming. We hypothesize that lack of control over these costly energetic processes results in decreased growth rate and fitness. In addition, our findings suggest a relationship between swarming and virulence in plant pathogens.

SUBMITTER: Koiv V

PROVIDER: S-EPMC3553148 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae.

Kõiv Viia V Andresen Liis L Broberg Martin M Frolova Jekaterina J Somervuo Panu P Auvinen Petri P Pirhonen Minna M Tenson Tanel T Mäe Andres A

PloS one 20130123 1

The posttranscriptional regulator RsmA controls the production of plant cell wall degrading enzymes (PCWDE) and cell motility in the Pectobacterium genus of plant pathogens. In this study the physiological role of gene regulation by RsmA is under investigation. Disruption of rsmA gene of the Pectobacterium wasabiae strain, SCC3193 resulted in 3-fold decrease in growth rate and increased virulence. The comparison of mRNA levels of the rsmA(-) mutant and wild-type using a genome-wide microarray sh ...[more]

PMID: 23372695

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Project description:BackgroundAlong the root axis of Arabidopsis thaliana, cells pass through different developmental stages. In the apical meristem repeated cycles of division increase the numbers of cells. Upon leaving the meristem, these cells pass the transition zone where they are physiologically and mechanically prepared to undergo subsequent rapid elongation. During the process of elongation epidermal cells increase their length by 300% in a couple of hours. When elongation ceases, the cells acquire their final size, shape and functions (in the differentiation zone). Ethylene administered as its precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is capable of inhibiting elongation in a concentration-dependent way. Using a microarray analysis, genes and/or processes involved in this elongation arrest are identified.ResultsUsing a CATMA-microarray analysis performed on control and 3h ACC-treated roots, 240 differentially expressed genes were identified. Quantitative Real-Time RT-PCR analysis of the 10 most up and down regulated genes combined with literature search confirmed the accurateness of the analysis. This revealed that inhibition of cell elongation is, at least partly, caused by restricting the events that under normal growth conditions initiate elongation and by increasing the processes that normally stop cellular elongation at the end of the elongation/onset of differentiation zone.ConclusionsACC interferes with cell elongation in the Arabidopsis thaliana roots by inhibiting cells from entering the elongation process and by immediately stimulating the formation of cross-links in cell wall components, diminishing the remaining elongation capacity. From the analysis of the differentially expressed genes, it becomes clear that many genes identified in this response, are also involved in several other kind of stress responses. This suggests that many responses originate from individual elicitors, but that somewhere in the downstream signaling cascade, these are converged to a 'common pathway'. Furthermore, several potential keyplayers, such as transcription factors and auxin-responsive genes, were identified by the microarray analysis. They await further analysis to reveal their exact role in the control of cell elongation.

Project description:Posttranscriptional regulator RsmA is part of a regulatory system that controls production of plant cell wall degrading enzymes (PCWDEs), motility and other virulence factors among the Pectobacterium spp of plant pathogens. We constructed the knockout mutation of rsmA gene in Pectobacterium wasabiae strain SCC3193. The rsmA- strain has three times lower growth rate but increased virulence when compared to wild type. To explain this phenotype we compared wild type and rsmA- mRNA levels using genome wide microarray. We found that the synthesis of all known virulence factors and flagella is upregulated, while cell division and peptidoglycan synthesis is down regulated in rsmA- strain. The TCA cycle is directed fully to energy production, indicating low energetic status of the cell that is a probable reason for the low growth rate of the mutant. Growth experiments showed that the enzymatic activities of extracellular virulence factors polygalacturonase and pectate lyase are very high throughout the growth curve even without induction by plant component. Wild type cells are rod shaped in liquid media, but elongated and hyperflagellated in swarm plate containing potato tuber extract and in potato tuber. The rsmA- strain exhibits the same conditional phenotype, but differentiation into swarmer cells is faster and cell elongation more pronounced. Virulence experiments in potato tuber showed that although rsmA- strain causes bigger tissue maceration, its ability to compete with the natural bacterial community in the host is decreased. We conclude that the lack of RsmA switches the cells to infective phenotype characterized by expression of virulence factors and swarming. The lack of control over these energy costly processes is probably the reason for decreased growth rate and fitness. Gene expression analysis from P. wasabie SCC3193 wildtype and SCC3193 rsmA mutant was performed on RNA samples extraxcted from the rsmA mutant (at 40 and 48 hours) and wildtype (at 24 hours). The strain were grown on 1.5% agar M9 minimal media plates supplemented with 10% potato extract. Three biological replicates were used from each strain at each time point.

Dataset Information

Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae.

Publications

Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae.

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