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An AlgU-Regulated Antisense Transcript Encoded within the Pseudomonas syringae fleQ Gene Has a Positive Effect on Motility.

ABSTRACT: Production of bacterial flagella is controlled by a multitiered regulatory system that coordinates the expression of 40 to 50 subunits and ordered assembly of these elaborate structures. Flagellar expression is environmentally controlled, presumably to optimize the benefits and liabilities of having these organelles on cell growth and survival. We recently reported a global survey of AlgU-dependent regulation and binding in Pseudomonas syringae pv. tomato DC3000 that included evidence for strong downregulation of many flagellar and chemotaxis motility genes. Here, we returned to those data to look for other AlgU-dependent influences on the flagellar regulatory network. We identified an AlgU-dependent antisense transcript expressed from within the fleQ gene, the master regulator of flagellar biosynthesis in Pseudomonas We tested whether expression of this antisense RNA influenced bacterial behavior and found that it reduces AlgU-dependent downregulation of motility. Importantly, this antisense expression influenced motility only under conditions in which AlgU was expressed. Comparative sequence analysis of the locus containing the antisense transcript's AlgU-dependent promoter in over 300 Pseudomonas genomes revealed sequence conservation in most strains that encode AlgU. This suggests that the antisense transcript plays an important role that is conserved across most of the genus Pseudomonas IMPORTANCE Pseudomonas syringae is a globally distributed host-specific bacterial pathogen that causes disease in a wide-range of plants. An elaborate gene expression regulation network controls flagellum production, which is important for proper flagellum assembly and a key aspect of certain lifestyle transitions. P. syringae pv. tomato DC3000 uses flagellum-powered motility in the early stages of host colonization and adopts a sessile lifestyle after entering plant tissues, but the regulation of this transition is not understood. Our work demonstrates a link between regulation of motility and global transcriptional control that facilitates bacterial growth and disease in plants. Additionally, sequence comparisons suggest that this regulation mechanism is conserved in most members of the genus Pseudomonas.

SUBMITTER: Markel E

PROVIDER: S-EPMC5847652 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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An AlgU-Regulated Antisense Transcript Encoded within the Pseudomonas syringae <i>fleQ</i> Gene Has a Positive Effect on Motility.

Markel Eric E Dalenberg Hollie H Monteil Caroline L CL Vinatzer Boris A BA Swingle Bryan B

Journal of bacteriology 20180312 7

Production of bacterial flagella is controlled by a multitiered regulatory system that coordinates the expression of 40 to 50 subunits and ordered assembly of these elaborate structures. Flagellar expression is environmentally controlled, presumably to optimize the benefits and liabilities of having these organelles on cell growth and survival. We recently reported a global survey of AlgU-dependent regulation and binding in <i>Pseudomonas syringae</i> pv. tomato DC3000 that included evidence for ...[more]

PMID: 29311280

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Project description:UnlabelledPlant-pathogenic bacteria are able to integrate information about their environment and adjust gene expression to provide adaptive functions. AlgU, an extracytoplasmic function (ECF) sigma factor encoded by Pseudomonas syringae, controls expression of genes for alginate biosynthesis and genes involved with resisting osmotic and oxidative stress. AlgU is active while these bacteria are associated with plants, where its presence supports bacterial growth and disease symptoms. We found that AlgU is an important virulence factor for P. syringae pv. tomato DC3000 but that alginate production is dispensable for disease in host plants. This implies that AlgU regulates additional genes that facilitate bacterial pathogenesis. We used transcriptome sequencing (RNA-seq) to characterize the AlgU regulon and chromatin immunoprecipitation sequencing (ChIP-seq) to identify AlgU-regulated promoters associated with genes directly controlled by this sigma factor. We found that in addition to genes involved with alginate and osmotic and oxidative stress responses, AlgU regulates genes with known virulence functions, including components of the Hrp type III secretion system, virulence effectors, and the hrpL and hrpRS transcription regulators. These data suggest that P. syringae pv. tomato DC3000 has adapted to use signals that activate AlgU to induce expression of important virulence functions that facilitate survival and disease in plants.ImportancePlant immune systems produce antimicrobial and bacteriostatic conditions in response to bacterial infection. Plant-pathogenic bacteria are adapted to suppress and/or tolerate these conditions; however, the mechanisms controlling these bacterial systems are largely uncharacterized. The work presented here provides a mechanistic explanation for how P. syringae pv. tomato DC3000 coordinates expression of multiple genetic systems, including those dedicated to pathogenicity, in response to environmental conditions. This work demonstrates the scope of AlgU regulation in P. syringae pv. tomato DC3000 and characterizes the promoter sequence regulated by AlgU in these bacteria.

Project description:The Pseudomonas syringae complex comprises different genetic groups that include strains from both agricultural and environmental habitats. This complex group has been used for decades as a "hodgepodge," including many taxonomically related species. More than 60 pathovars of P. syringae have been described based on distinct host ranges and disease symptoms they cause. These pathovars cause disease relying on an array of virulence mechanisms. However, P. syringae pv. syringae (Pss) is the most polyphagous bacterium in the P. syringae complex, based on its wide host range, that primarily affects woody and herbaceous host plants. In early 1990s, bacterial apical necrosis (BAN) of mango trees, a critical disease elicited by Pss in Southern Spain was described for the first time. Pss exhibits important epiphytic traits and virulence factors, which may promote its survival and pathogenicity in mango trees and in other plant hosts. Over more than two decades, Pss strains isolated from mango trees have been comprehensively investigated to elucidate the mechanisms that governs their epiphytic and pathogenic lifestyles. In particular, the vast majority of Pss strains isolated from mango trees produce an antimetabolite toxin, called mangotoxin, whose leading role in virulence has been clearly demonstrated. Moreover, phenotypic, genetic and phylogenetic approaches support that Pss strains producers of BAN symptoms on mango trees all belong to a single phylotype within phylogroup 2, are adapted to the mango host, and produce mangotoxin. Remarkably, a genome sequencing project of the Pss model strain UMAF0158 revealed the presence of other factors that may play major roles in its different lifestyles, such as the presence of two different type III secretion systems, two type VI secretion systems and an operon for cellulose biosynthesis. The role of cellulose in increasing mango leaf colonization and biofilm formation, and impairing virulence of Pss, suggests that cellulose may play a pivotal role with regards to the balance of its different lifestyles. In addition, 62-kb plasmids belonging to the pPT23A-family of plasmids (PFPs) have been strongly associated with Pss strains that inhabit mango trees. Further, complete sequence and comparative genomic analyses revealed major roles of PFPs in detoxification of copper compounds and ultraviolet radiation resistance, both improving the epiphytic lifestyle of Pss on mango surfaces. Hence, in this review we summarize the research that has been conducted on Pss by our research group to elucidate the molecular mechanisms that underpin the epiphytic and pathogenic lifestyle on mango trees. Finally, future directions in this particular plant-pathogen story are discussed.

Dataset Information

An AlgU-Regulated Antisense Transcript Encoded within the Pseudomonas syringae fleQ Gene Has a Positive Effect on Motility.

Publications

An AlgU-Regulated Antisense Transcript Encoded within the Pseudomonas syringae <i>fleQ</i> Gene Has a Positive Effect on Motility.

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