Deletion of bglC triggers a genetic compensation response by awakening the expression of alternative beta-glucosidase

Deflandre, Benoit; Thiébaut, Noémie; Planckaert, Sören; Jourdan, Samuel; Anderssen, Sinaeda; Hanikenne, Marc; Devreese, Bart; Francis, Isolde M.; Rigali, Sébastien

doi:10.1016/j.bbagrm.2020.194615

Cited by 15 publications

(43 citation statements)

References 40 publications

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“…Also, the interference with thaxtomin production caused by the inactivation of the cellobiose and cellotriose beta-glucosidase BglC (41) revealed a genetic compensation phenomenon that awakened the expression of alternative beta-glucosidases allowing S . scabiei to maintain the capacity to use cello- oligosaccharides (42). The experimental set-ups can also sometimes be suboptimal – such as inappropriate host and/or culture conditions – to observe the real impact of a mutation and therefore to conclude on the role of a gene product in a biological process.…”

Section: Discussionmentioning

confidence: 99%

The virulome ofStreptomyces scabieiin response to cello-oligosaccharides elicitors

Deflandre

Stulanivic

Planckaert

et al. 2021

Preprint

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The development of spots or lesions symptomatic of the common scab disease on root and tuber crops is caused by few pathogenic Streptomyces with Streptomyces scabiei 87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production in S. scabiei is in turn boosted by the cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism of S. scabiei 87-22 show a production and/or transcriptional response to cello-oligosaccharides. Comparative metabolomic and transcriptomic analyses revealed that molecules of the virulome of S. scabiei induced by cellobiose and cellotriose include i) thaxtomins and concanamycins phytotoxins (and to a lesser extent N-coronafacoyl-L-isoleucine), ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, iii) ectoine for protection against osmotic shock once inside the host, and iv) bottromycins and concanamycins antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cell-oligosaccharides reduced the production of the spore germination inhibitors germicidins and the plant growth regulators rotihibins. The metabolomic study also revealed that cellotriose is in general a more potent elicitor of the virulome compared to cellobiose. This result supports an earlier hypothesis that suggested that the trisaccharide would be the real virulence-triggering factor released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of another master regulator sensing the internalization of cello-oligosaccharides. Finally, we found nine additional cryptic and orphan BGCs that have their expression awakened by cello-oligosaccharides, demonstrating that other and yet to be discovered metabolites are part of the virulome of S. scabiei.

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Section: Discussionmentioning

confidence: 99%

The virulome ofStreptomyces scabieiin response to cello-oligosaccharides elicitors

Deflandre

Stulanivic

Planckaert

et al. 2021

Preprint

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“…The intensity of the competition might be dependent on the quality of available SOM [29,112,114]. Some of these oligosaccharides also act as environmental signals to plant pathogenic Streptomyces inducing the production of thaxtomin [117] so that they may further support their pathogenicity, but the regulation of those pathways is not completely resolved [119].…”

Section: Organic Matter Modifies Microbial Communities and Increases mentioning

confidence: 99%

Micronutrients and Soil Microorganisms in the Suppression of Potato Common Scab

et al. 2021

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Nature-friendly approaches for crop protection are sought after in the effort to reduce the use of agrochemicals. However, the transfer of scientific findings to agriculture practice is relatively slow because research results are sometimes contradictory or do not clearly lead to applicable approaches. Common scab of potatoes is a disease affecting potatoes worldwide, for which no definite treatment is available. That is due to many complex interactions affecting its incidence and severity. The review aims to determine options for the control of the disease using additions of micronutrients and modification of microbial communities. We propose three approaches for the improvement by (1) supplying soils with limiting nutrients, (2) supporting microbial communities with high mineral solubilization capabilities or (3) applying communities antagonistic to the pathogen. The procedures for the disease control may include fertilization with micronutrients and appropriate organic matter or inoculation with beneficial strains selected according to local environmental conditions. Further research is proposed to use metagenomics/metabolomics to identify key soil–plant–microbe interactions in comparisons of disease-suppressive and -conducive soils.

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“…BglC of S. scabiei 87-22 with a six-histidine tag fused to the N-terminus part of the protein (His 6 -BglC) was produced in Escherichia coli BL21(DE3) Rosetta™ and purified by nickel affinity chromatography as already described in [10,11]. The pure protein was stored and used in HEPES buffer (50 mM, pH 7.5).…”

Section: Heterologous Production Of His 6 -Tagged Proteins and Purificationmentioning

confidence: 99%

“…Finally, we discovered that the primary function of bglC/BglC, i.e., the utilization of cellooligosaccharides, is safeguarded by a mechanism of genetic compensation that awakens the expression of alternative beta-glucosidases upon perceiving the loss of bglC [11]. When BglC is active, the transcription of these alternative beta-glucosidases is kept to a minimal level and is not induced by cello-oligosaccharides (Figure 1, role ).…”

Section: Introductionmentioning

confidence: 99%

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BglC of Streptomyces scabiei is a scopolin-hydrolyzing β-glucosidase interfering with the host defense mechanism

Deflandre

Rigali

2021

Preprint

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The beta-glucosidase BglC fulfills multiple functions in both primary metabolism and induction of pathogenicity of Streptomyces scabiei, the causative agent of the common scab disease of root and tuber crops. Indeed, this enzyme hydrolyzes cellobiose and cellotriose to directly feed glycolysis with glucose, but also modifies the intracellular concentration of these cello-oligosaccharides which are the virulence elicitors. The inactivation of bglC also led to unexpected phenotypes such as the constitutive overproduction of thaxtomin A, the main virulence determinant of S. scabiei. In this work we revealed a new target substrate of BglC, the phytoalexin scopolin. Removal of the glucose moiety of scopolin generates scopoletin, a potent inhibitor of thaxtomin A production. The hydrolysis of scopolin by BglC presents substrate inhibition kinetics which contrasts with the typical Michaelis–Menten saturation curve previously observed for the degradation of its natural substrate cellobiose. Our work therefore reveals that BglC targets both cello-oligosaccharide elicitors emanating from the hosts of S. scabiei, and the scopolin phytoalexin generated by the host defense mechanisms, thereby occupying a key position to fine-tune the production of the main virulence determinant thaxtomin A.

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Deletion of bglC triggers a genetic compensation response by awakening the expression of alternative beta-glucosidase

Cited by 15 publications

References 40 publications

The virulome ofStreptomyces scabieiin response to cello-oligosaccharides elicitors

The virulome ofStreptomyces scabieiin response to cello-oligosaccharides elicitors

Micronutrients and Soil Microorganisms in the Suppression of Potato Common Scab

BglC of Streptomyces scabiei is a scopolin-hydrolyzing β-glucosidase interfering with the host defense mechanism

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