A gossypol biosynthetic intermediate disturbs plant defence response

Abstract

Plant secondary metabolites and their biosynthesis have attracted great interest, but investigations of the activities of hidden intermediates remain rare. Gossypol and related sesquiterpenes are the major phytoalexins in cotton. Among the six biosynthetic intermediates recently identified, 8-hydroxy-7-keto-d-cadinene (C234) crippled the plant disease resistance when accumulated upon gene silencing. C234 harbours an a,b-unsaturated carbonyl thus is a reactive electrophile species. Here, we show that C234 application also dampened the Arabidopsis resistance against the bacterial pathogen Pseudomonas syringae pv. maculicola (Psm). We treated Arabidopsis with C234, Psm and (PsmþC234), and analysed the leaf transcriptomes. While C234 alone exerted a mild effect, it greatly stimulated an over-response to the pathogen. Of the 7335 genes affected in the (PsmþC234)-treated leaves, 3476 were unresponsive without the chemical, in which such functional categories as 'nucleotides transport', 'vesicle transport', 'MAP kinases', 'G-proteins', 'protein assembly and cofactor ligation' and 'light reaction' were enriched, suggesting that C234 disturbed certain physiological processes and the protein complex assembly, leading to distorted defence response and decreased disease resistance. As C234 is efficiently metabolized by CYP71BE79, plants of cotton lineage have evolved a highly active enzyme to prevent the phytotoxic intermediate accumulation during gossypol pathway evolution.