Cell wall integrity and high osmolarity glycerol pathways are required for adaptation of Alternaria brassicicola to cell wall stress caused by brassicaceous indolic phytoalexins

Abstract

SummaryCamalexin, the characteristic phytoalexin of Arabidopsis thaliana, inhibits growth of the fungal necrotroph Alternaria brassicicola. This plant metabolite probably exerts its antifungal toxicity by causing cell membrane damage. Here we observed that activation of a cellular response to this damage requires cell wall integrity (CWI) and the high osmolarity glycerol (HOG) pathways. Camalexin was found to activate both AbHog1 and AbSlt2 MAP kinases, and activation of the latter was abrogated in a AbHog1 deficient strain. Mutant strains lacking functional MAP kinases showed hypersensitivity to camalexin and brassinin, a structurally related phytoalexin produced by several cultivated Brassica species. Enhanced susceptibility to the membrane permeabilization activity of camalexin was observed for MAP kinase deficient mutants. These results suggest that the two signalling pathways have a pivotal role in regulating a cellular compensatory response to preserve cell integrity during exposure to camalexin. AbHog1 and AbSlt2 deficient mutants had reduced virulence on host plants that may, at least for the latter mutants, partially result from their inability to cope with defence metabolites such as indolic phytoalexins. This constitutes the first evidence that a phytoalexin activates fungal MAP kinases and that outputs of activated cascades contribute to protecting the fungus against antimicrobial plant metabolites.

Characterization of glutathione transferases involved in the pathogenicity of Alternaria brassicicola

“…The pathogenicity of A. brassicicola could be partly related to its ability to protect itself against Brassicaceae defenses compounds including ITC [23–25]. The results obtained by [5, 26] showed that at least six genes encoding GST in A. brassicicola , were up-regulated upon exposure to ITC.…”

Mitogen-Activated Protein Kinase Signaling in Plant-Interacting Fungi: Distinct Messages from Conserved Messengers

“…In the necrotroph A. brassicicola, the cellular response elicited by such damage requires both the cell wall integrity and HOG pathways, leading to the activation of fungal MAPKs Abr-Slt2 and Abr-Hog1, respectively (Joubert et al, 2011). Alternaria strains lacking these MAPKs are not only hypersensitive to camalexin, but also to brassinin, a structurally related phytoalexin from Brassica species (Joubert et al, 2011).…”

“…In the necrotroph A. brassicicola, the cellular response elicited by such damage requires both the cell wall integrity and HOG pathways, leading to the activation of fungal MAPKs Abr-Slt2 and Abr-Hog1, respectively (Joubert et al, 2011). Alternaria strains lacking these MAPKs are not only hypersensitive to camalexin, but also to brassinin, a structurally related phytoalexin from Brassica species (Joubert et al, 2011). In F. graminearum, two MAPKs, Fgr-Kss1 and Fgr-Slt2, appear to play a major role in fungal sensitivity to certain plant defensins, a small family of pathogenesis-related proteins ( Figure 7; Ramamoorthy et al, 2007).…”

New Antimicrobial Agents of Plant Origin

“…In vivo antimicrobial activity has only been demonstrated for camalexin in Arabidopsis, with enhanced susceptibility to fungal pathogens in mutants unable to produce this compound (Schlaeppi et al 2010;Stotz et al 2011). Camalexin is a lipophilic molecule and its mechanism of action, while not well understood, appears to involve membrane disruption in both fungi and bacteria (Rogers et al 1996;Joubert et al 2011;Ahuja et al 2012). In fungi camalexin treatment activates cell wall integrity and high osmolarity pathways that contribute to pathogen virulence.…”