Glucosinolate-derived isothiocyanates impact mitochondrial function in fungal cells and elicit an oxidative stress response necessary for growth recovery.

Benoit Calmes,Claire Campion,Thomas Guillemette,Bã©Atrice Iacomi,Guillaume Nâ€™Guyen,Jã©Rome Dumur,Philippe Simoneau,Eva Dias,David Macherel,Carlos A Brisach,Sandrine Pignã©

doi:10.3389/fpls.2015.00414

Abstract

Glucosinolates are brassicaceous secondary metabolites that have long been considered as chemical shields against pathogen invasion. Isothiocyanates (ITCs), are glucosinolate-breakdown products that have negative effects on the growth of various fungal species. We explored the mechanism by which ITCs could cause fungal cell death using Alternaria brassicicola, a specialist Brassica pathogens, as model organism. Exposure of the fungus to ICTs led to a decreased oxygen consumption rate, intracellular accumulation of reactive oxygen species (ROS) and mitochondrial-membrane depolarization. We also found that two major regulators of the response to oxidative stress, i.e., the MAP kinase AbHog1 and the transcription factor AbAP1, were activated in the presence of ICTs. Once activated by ICT-derived ROS, AbAP1 was found to promote the expression of different oxidative-response genes. This response might play a significant role in the protection of the fungus against ICTs as mutants deficient in AbHog1 or AbAP1 were found to be hypersensitive to these metabolites. Moreover, the loss of these genes was accompanied by a significant decrease in aggressiveness on Brassica. We suggest that the robust protection response against ICT-derived oxidative stress might be a key adaptation mechanism for successful infection of host plants by Brassicaceae-specialist necrotrophs like A. brassicicola.

Highlights

Plants- as part of their overall defense arsenal- counter pathogen attack by producing de novo antimicrobial phytoalexins (Hammerschmidt, 1999; Ahuja et al, 2012)
Analyses of growth curves in liquid medium supplemented with various concentrations of Al-ITC, Bz-ITC, or Ph-ITC were used to assess the susceptibility of the WT A. brassicicola strain Abra43 to different ICTs
Glucosinolates are a class of S- and N- containing secondary metabolites that are found in only 15 botanical families of the Capparales order and are very abundant in the Brassicaceae family (Fahey et al, 2001)

Summary

Introduction

Plants- as part of their overall defense arsenal- counter pathogen attack by producing de novo antimicrobial phytoalexins (Hammerschmidt, 1999; Ahuja et al, 2012). Besides these newly synthesized metabolites, many plant species constitutively accumulate compounds referred to as phytoanticipins (Osbourn, 1996) that, due to their high concentration in tissues and potential antimicrobial activities, may contribute to protecting the plant from pathogen infection. Phytoanticipins are a very heterogeneous group of molecules with high structural diversity and the basis of their biocidal activity on fungal cells may not be unique. Allicin is readily taken up by fungal cells and, due to its oxidizing properties, might activate apoptosis (Gruhlke et al, 2010)

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