Trading acyls and swapping sugars: metabolic innovations in Solanum 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. We characterized trichome acylsugars of the Clade II species Solanum melongena (brinjal eggplant) using liquid chromatography-mass spectrometry (LC-MS), gas chromatography-MS and nuclear magnetic resonance (NMR) spectroscopy. This led to the identification of eight unusual structures with inositol or inositol glycoside cores, and hydroxyacyl chains. LC-MS analysis of 31 species in the megadiverse Solanum genus revealed striking acylsugar diversity with some traits restricted to specific clades and species. Acylinositols were found throughout each clade while acylglucoses were restricted to DulMo and VANAns species. Medium length hydroxyacyl chains were identified in many species. Analysis of tissue-specific transcriptomes and interspecific acylsugar acetylation differences led to the unexpected identification of the S. melongena 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 Solanum acylsugar structures and harnessing this diversity in breeding and synthetic biology.