Current Biology
Volume 30, Issue 16, 17 August 2020, Pages 3130-3140.e6
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Article
Thiosulfinate Tolerance Is a Virulence Strategy of an Atypical Bacterial Pathogen of Onion

https://doi.org/10.1016/j.cub.2020.05.092Get rights and content
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Highlights

  • Pantoea ananatis lacks typical virulence-associated protein secretion systems

  • The Pantoea ananatis alt gene cluster confers tolerance to Allium thiosulfinates

  • Colonization of necrotized onion tissue requires the alt gene cluster

  • Pathogen-induced cell death and thiosulfinate tolerance support onion necrotrophy

Summary

Unlike most characterized bacterial plant pathogens, the broad-host-range plant pathogen Pantoea ananatis lacks both the virulence-associated type III and type II secretion systems. In the absence of these typical pathogenicity factors, P. ananatis induces necrotic symptoms and extensive cell death in onion tissue dependent on the HiVir proposed secondary metabolite synthesis gene cluster. Onion (Allium. cepa L), garlic (A. sativum L.), and other members of the Allium genus produce volatile antimicrobial thiosulfinates upon cellular damage. However, the roles of endogenous thiosulfinate production in host-bacterial pathogen interactions have not been described. We found a strong correlation between the genetic requirements for P. ananatis to colonize necrotized onion tissue and its capacity for tolerance to the thiosulfinate “allicin” based on the presence of an eleven-gene, plasmid-borne, virulence cluster of sulfur redox genes. We have designated them “alt” genes for allicin tolerance. We show that allicin and onion thiosulfinates restrict bacterial growth with similar kinetics. The alt gene cluster is sufficient to confer allicin tolerance and protects the glutathione pool during allicin treatment. Independent alt genes make partial phenotypic contributions indicating that they function as a collective cohort to manage thiol stress. Our work implicates endogenous onion thiosulfinates produced during cellular damage as major mediators of interactions with bacteria. The P. ananatis-onion pathosystem can be modeled as a chemical arms race of pathogen attack, host chemical counterattack, and pathogen defense.

Keywords

plant-pathogen interactions
allicin
thiosulfinate
Pantoea ananatis
onion
evolutionary arms race, virulence mechanism

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