Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity

The chloroplast is a critical battleground in the arms race between plants and pathogens. Among microbe-secreted mycotoxins, tenuazonic acid (TeA), produced by the genus Alternaria and other phytopathogenic fungi, inhibits photosynthesis, leading to a burst of photosynthetic singlet oxygen (¹O₂) that is implicated in damage and chloroplast-to-nucleus retrograde signaling. Despite the significant crop damage caused by Alternaria pathogens, our understanding of the molecular mechanism by which TeA promotes pathogenicity and cognate plant defense responses remains fragmentary. We now reveal that A. alternata induces necrotrophic foliar lesions by harnessing EXECUTER1 (EX1)/EX2-mediated chloroplast-to-nucleus retrograde signaling activated by TeA toxin-derived photosynthetic ¹O₂ in Arabidopsis thaliana. Mutation of the ¹O₂-sensitive EX1-W643 residue or complete deletion of the EX1 singlet oxygen sensor domain compromises expression of ¹O₂-responsive nuclear genes and foliar lesions. We also found that TeA toxin rapidly induces nuclear genes implicated in jasmonic acid (JA) synthesis and signaling, and EX1-mediated retrograde signaling appears to be critical for establishing a signaling cascade from ¹O₂ to JA. The present study sheds new light on the foliar pathogenicity of A. alternata, during which EX1-dependent ¹O₂ signaling induces JA-dependent foliar cell death.