Dataset Information

Contribution of the ?-glucosidase BglC to the onset of the pathogenic lifestyle of Streptomyces scabies.

ABSTRACT: Common scab disease on root and tuber plants is caused by Streptomyces scabies and related species which use the cellulose synthase inhibitor thaxtomin A as the main phytotoxin. Thaxtomin production is primarily triggered by the import of cello-oligosaccharides. Once inside the cell, the fate of the cello-oligosaccharides is dichotomized: (i) the fuelling of glycolysis with glucose for the saprophytic lifestyle through the action of ?-glucosidase(s) (BGs); and (ii) elicitation of the pathogenic lifestyle by the inhibition of CebR-mediated transcriptional repression of thaxtomin biosynthetic genes. Here, we investigated the role of scab57721, encoding a putative BG (BglC), in the onset of the pathogenicity of S. scabies. Enzymatic assays showed that BglC was able to release glucose from cellobiose, cellotriose and all other cello-oligosaccharides tested. Its inactivation resulted in a phenotype opposite to that expected, as reduced production of thaxtomin was monitored when the mutant was cultivated on medium containing cello-oligosaccharides as unique carbon source. This unexpected phenotype could be attributed to the highly increased activity of alternative intracellular BGs, probably as a compensation for bglC inactivation, which then prevented cellobiose and cellotriose accumulation to reduce the activity of CebR. In contrast, when the bglC null mutant was cultivated on medium devoid of cello-oligosaccharides, it instead constitutively produced thaxtomin. This observed hypervirulent phenotype does not fit with the proposed model of the cello-oligosaccharide-mediated induction of thaxtomin production, and suggests that the role of BglC in the route to the pathogenic lifestyle of S. scabies is more complex than currently presented.

SUBMITTER: Jourdan S

PROVIDER: S-EPMC6638027 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Contribution of the β-glucosidase BglC to the onset of the pathogenic lifestyle of Streptomyces scabies.

Jourdan Samuel S Francis Isolde M IM Deflandre Benoit B Tenconi Elodie E Riley Jennifer J Planckaert Sören S Tocquin Pierre P Martinet Loïc L Devreese Bart B Loria Rosemary R Rigali Sébastien S

Molecular plant pathology 20171226 6

Common scab disease on root and tuber plants is caused by Streptomyces scabies and related species which use the cellulose synthase inhibitor thaxtomin A as the main phytotoxin. Thaxtomin production is primarily triggered by the import of cello-oligosaccharides. Once inside the cell, the fate of the cello-oligosaccharides is dichotomized: (i) the fuelling of glycolysis with glucose for the saprophytic lifestyle through the action of β-glucosidase(s) (BGs); and (ii) elicitation of the pathogenic ...[more]

PMID: 29077242

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Project description:UNLABELLED:A relatively small number of species in the large genus Streptomyces are pathogenic; the best characterized of these is Streptomyces scabies. The pathogenicity of S. scabies strains is dependent on the production of the nitrated diketopiperazine thaxtomin A, which is a potent plant cellulose synthesis inhibitor. Much is known about the genetic loci associated with plant virulence; however, the molecular mechanisms by which S. scabies triggers expression of thaxtomin biosynthetic genes, beyond the pathway-specific activator TxtR, are not well understood. In this study, we demonstrate that binding sites for the cellulose utilization repressor CebR occur and function within the thaxtomin biosynthetic cluster. This was an unexpected result, as CebR is devoted to primary metabolism and nutritive functions in nonpathogenic streptomycetes. In S. scabies, cellobiose and cellotriose inhibit the DNA-binding ability of CebR, leading to an increased expression of the thaxtomin biosynthetic and regulatory genes txtA, txtB, and txtR. Deletion of cebR results in constitutive thaxtomin A production and hypervirulence of S. scabies. The pathogenicity of S. scabies is thus under dual direct positive and negative transcriptional control where CebR is the cellobiose-sensing key that locks the expression of txtR, the key necessary to unlock the production of the phytotoxin. Interestingly, CebR-binding sites also lie upstream of and within the thaxtomin biosynthetic clusters in Streptomyces turgidiscabies and Streptomyces acidiscabies, suggesting that CebR is most likely an important regulator of virulence in these plant-pathogenic species as well. IMPORTANCE:What makes a microorganism pathogenic is not limited to the genes acquired for virulence. Using the main causative agent of scab lesions on root and tuber crops as an example, our work identified the subtle but essential genetic changes that generate the cis-acting elements necessary for proper timing of the expression of the cluster of genes responsible for the biosynthesis of thaxtomin A, the primary virulence factor in plant-pathogenic streptomycetes. These data illustrate a situation in which a regulator associated with primary metabolism in nonpathogens, CebR, has been coopted as a master regulator of virulence in pathogenic species. Furthermore, the manipulation of CebR-mediated control of thaxtomin production will facilitate overproduction of this natural and biodegradable herbicide for commercial purposes. Our work thus provides a concrete example of how a strictly theoretical and computational work was able to elucidate a regulatory mechanism associated with the virulence of a plant pathogen and to generate solutions to purely agro-industrial concerns.

Dataset Information

Contribution of the ?-glucosidase BglC to the onset of the pathogenic lifestyle of Streptomyces scabies.

Publications

Contribution of the β-glucosidase BglC to the onset of the pathogenic lifestyle of Streptomyces scabies.

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