Deficiencies in Jasmonate-Mediated Plant Defense Reveal Quantitative Variation in Botrytis cinerea Pathogenesis

Abstract

Despite the described central role of jasmonate signaling in plant defense against necrotrophic pathogens, the existence of intraspecific variation in pathogen capacity to activate or evade plant jasmonate-mediated defenses is rarely considered. Experimental infection of jasmonate-deficient and jasmonate-insensitive Arabidopsis thaliana with diverse isolates of the necrotrophic fungal pathogen Botrytis cinerea revealed pathogen variation for virulence inhibition by jasmonate-mediated plant defenses and induction of plant defense metabolites. Comparison of the transcriptional effects of infection by two distinct B. cinerea isolates showed only minor differences in transcriptional responses of wild-type plants, but notable isolate-specific transcript differences in jasmonate-insensitive plants. These transcriptional differences suggest B. cinerea activation of plant defenses that require plant jasmonate signaling for activity in response to only one of the two B. cinerea isolates tested. Thus, similar infection phenotypes observed in wild-type plants result from different signaling interactions with the plant that are likely integrated by jasmonate signaling.

Author Summary

While many important elements of plant defense signaling have been identified, the function of these defense signaling pathways may mask additional variation in the plant–pathogen interaction, including both pathogen variation and variation in downstream plant defense responses. Jasmonate plant hormones contribute to both plant development and defense, including plant defense against necrotrophic fungal pathogens such as the grey mold Botrytis cinerea. Ten diverse B. cinerea isolates all showed increased virulence and decreased induction of a plant antimicrobial metabolite in experimental infections of Arabidopsis thaliana lacking functional jasmonate signaling. Yet within this consistent result, B. cinerea isolates varied considerably. Through comparing the transcript profiles of A. thaliana infected with the two most disparate B. cinerea isolates, we found that wild-type plants showed similar transcriptional responses to infection with these two isolates, but the absence of functional jasmonate signaling revealed dramatic differences in plant response, including groups of co-regulated genes that may participate in undescribed plant response networks. Jasmonate signaling appears to integrate plant responses to diverse pathogen inputs, and its absence may reveal novel aspects of plant–pathogen interaction.