Elevated temperature drives the biosynthesis of novel acylated glucosinolates in Arabidopsis thaliana seeds

Abstract

Glucosinolates (GSLs) are major defensive compounds massively accumulated in Brassicaceae seeds, including that of the model plant Arabidopsis thaliana. While most studies have focused on the role of GSL in responses to biotic stress, the potential regulation and function of GSLs in responses to abiotic stresses have been neglected, particularly in seeds. In this study, multi-omic analyses revealed a previously uncharacterized GSL modification pathway induced by elevated temperature (ET) during A. thaliana seed development. Activation of this pathway leads to the production of several novel thioglucose-acylated GSLs, including sinapoylated and benzoylated derivatives. A reverse genetics approach demonstrated that the SERINE CARBOXYPEPTIDASE-LIKE 17 (SCPL17) and BENZOYLOXYGLUCOSINOLATE 1 (BZO1) enzymes are required for the acylation of GSL thioglucose moieties. Furthermore, the accumulation of acylated GSLs in seeds of 85 A. thaliana accessions grown under standard condition was shown to correlate with the average annual temperature of their origin site, suggesting that thioglucose-acylated GSLs production may reflect long-term thermal adaptation across natural populations. Taken together, these results demonstrate that thioglucose acylation by SCPL17 and BZO1 represents a new layer of GSL diversification in A. thaliana seeds that contributes to both ET response and long-term environmental adaptation.