Phytosulfokine signalling blocks mycotoxin toxicity in Arabidopsis and mediates suppression of cell death activated by bacterial microbe-associated molecular patterns.

Fumonisin B1 (FB1) is a mycotoxin that disrupts ceramide biosynthesis and kills plants. Prior activation with bacterial microbe-associated molecular patterns (MAMPs), such as components of bacterial flagella, effectively suppresses FB1-induced cell death. The molecular basis of this defence against mycotoxin toxicity is poorly understood. Analysis of extracellular peptide receptors provided initial circumstantial evidence linking phytosulfokine (PSK) signalling with Arabidopsis thaliana responses to FB1. We used synthetic PSK peptides and quantitative proteomics to investigate this link and established the basis for peptide-induced Arabidopsis immunity to FB1. Exogenous PSK fully protected Arabidopsis plants from FB1 toxicity in wild-type plants, but not in loss-of-function mutants lacking PSK RECEPTOR 1 (PSKR1) or its co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1 (BAK1). Mutants lacking the precursor PSK-processing subtilase (SBT3.8) enzyme were more sensitive to FB1. The partial flagellin peptide flg22, which activates innate immunity to block FB1 toxicity in wild-type plants, failed to rescue pskr1 mutants, indicating that PSK signalling functions downstream of flg22. Proteomic analysis revealed Calvin cycle downregulation by FB1, while co-application of the toxin with PSK increased Calvin cycle capacity. Our study reveals that the mechanism of disabling mycotoxin toxicity by MAMPs is activation of PSK signalling and stimulation of the photosynthetic machinery.