A Novel Role for Phytosulfokine Signalling in Regulating Arabidopsis Responses to Fumonisin B1

Developing effective solutions to the challenge of plant diseases threatening global food security requires understanding pathogen-host interactions. Perception of pathogen-associated molecular patterns (PAMPs) by pattern recognition receptors (PRRs) activates PAMP-triggered immunity (PTI). Some fungal pathogens secrete mycotoxins to disable host defences and trigger cell death. Reports have shown that PTI activation blocks mycotoxin-induced cell death. The mechanism by which mycotoxins disable plant defences is poorly understood and how PTI protects plants from phytotoxic effects of mycotoxins has been unknown until now. To address this knowledge gap, we used an experimental system employing pathogen-free mycotoxin purified from Fusarium verticillioides and a synthetic 22 amino acid-long peptide (flg22) matching the conserved sequence found in bacterial flagella. We show that fumonisin B1 (FB1) disables Arabidopsis thaliana defences by downregulating the gene encoding BAK1 Brassinosteroid-insensitive 1-Associated Kinase 1, which dimerises with PAMP-specific receptors. These results suggest that mycotoxins weaken host defences by disrupting formation of functional receptor complexes for PAMP binding and PTI activation. However, when flg22 activates PTI prior to or concurrently with FB1 treatment, BAK1 expression is restored, and cell death is averted. This implies that timing of PAMP detection in relation to mycotoxin secretion is critical to the outcome of pathogen-host interactions. We also show that phytosulfokine (PSK) signalling, which is activated when the extracellular PSK peptide binds to PSK RECEPTOR 1 (PSKR1)-BAK1 receptor complex, blocks FB1-induced cell death. Co-treatment of Arabidopsis with FB1 and PSK blocked cell death in wildtype, but not loss-of-function bak1 or pskr1 mutants. Importantly, flg22 activated PSK signalling to protect Arabidopsis from FB1. Multi-omics analyses placed the Calvin cycle and iron homeostasis at the epicentre of FB1 and PSK signalling in controlling Arabidopsis defences. These findings advance our understanding of mycotoxin destruction of plant defences and highlight the importance of extracellular peptide signalling in stress-adaptive responses.