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 ((1)O(2)) 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 (1)O(2) in Arabidopsis thaliana. Mutation of the (1)O(2)-sensitive EX1-W643 residue or complete deletion of the EX1 singlet oxygen sensor domain compromises expression of (1)O(2)-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 (1)O(2) to JA. The present study sheds new light on the foliar pathogenicity of A. alternata, during which EX1-dependent (1)O(2) signaling induces JA-dependent foliar cell death.