Trading acyls and swapping sugars: metabolic innovations in trichomes.

Solanaceae (nightshade family) species synthesize a remarkable array of clade- and tissue-specific specialized metabolites. Protective acylsugars, one such class of structurally diverse metabolites, are produced by AcylSugar AcylTransferases from sugars and acyl-coenzyme A esters. Published research revealed trichome acylsugars composed of glucose and sucrose cores in species across the family. In addition, acylsugars were analyzed across a small fraction of the >1200 species in the phenotypically megadiverse genus, with a handful containing inositol and glycosylated inositol cores. The current study sampled several dozen species across subclades of the to get a more detailed view of acylsugar chemodiversity. In depth characterization of acylsugars from the Clade II species (brinjal eggplant) led to the identification of eight unusual structures with inositol or inositol glycoside cores, and hydroxyacyl chains. Liquid chromatography-mass spectrometry analysis of 31 additional species in the genus revealed striking acylsugar diversity with some traits restricted to specific clades and species. Acylinositols and inositol-based acyldisaccharides were detected throughout much of the genus. In contrast, acylglucoses and acylsucroses were more restricted in distribution. Analysis of tissue-specific transcriptomes and interspecific acylsugar acetylation differences led to the identification of the AcylSugar AcylTransferase 3-Like 1 (SmASAT3-L1; SMEL4.1_12g015780) enzyme. This enzyme is distinct from previously characterized acylsugar acetyltransferases, which are in the ASAT4 clade, and appears to be a functionally divergent ASAT3. This study provides a foundation for investigating the evolution and function of diverse acylsugar structures and harnessing this diversity in breeding and synthetic biology.