Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence

Summary

Botrytis cinerea is a fungus that causes plant disease by overcoming plant chemical defenses called saponins. Researchers discovered that this fungus uses four different molecular strategies to survive saponin exposure: it breaks down saponins with an enzyme, modifies membrane structures to resist saponin damage, activates proteins that protect the cell membrane, and repairs membrane damage after it occurs. These findings explain how this fungus successfully infects plants protected by saponins and reveal new understanding of how microorganisms resist antimicrobial compounds.

Background

Saponins are plant secondary metabolites with broad antimicrobial toxicity that serve as basal plant defense compounds against fungal pathogens. Previously, enzymatic deglycosylation was the only known fungal resistance mechanism against saponins. This study investigates multiple tolerance mechanisms in Botrytis cinerea, a broad host-range fungal pathogen.

Objective

To characterize the molecular mechanisms by which Botrytis cinerea establishes tolerance to saponins, specifically α-tomatine and digitonin, and how these mechanisms contribute to virulence on saponin-producing host plants. The study aims to identify both enzymatic and non-enzymatic resistance pathways.

Results

Four distinct cellular mechanisms for saponin tolerance were identified: a novel GH43 β-xylosidase (BcTOM1) for enzymatic deglycosylation, GT28 glycosyl transferases for sterol modification, RTA1-like proteins for membrane function, and PEF1 for membrane repair. These mechanisms act independently and together confer substantial tolerance to α-tomatine and digitonin.

Conclusion

Botrytis cinerea employs a multilayered defense strategy against saponins combining enzymatic degradation with three additional membrane-protective mechanisms. These findings reveal previously unknown non-hydrolytic mechanisms of saponin resistance and have implications for understanding fungal pathogenicity and resistance to antimicrobial compounds in other pathogenic systems.
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