Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato

Abstract

Plants produce myriad taxonomically restricted specialized metabolites. This diversity - and our ability to correlate genotype with phenotype - makes the evolution of these ecologically and medicinally important compounds interesting and experimentally tractable. Trichomes of tomato and other nightshade family plants produce structurally diverse protective compounds termed acylsugars. While cultivated tomato (Solanum lycopersicum) accumulates strictly acylsucroses, the South American wild relative Solanum pennellii produces copious amounts of acylglucoses. Genetic, transgenic and biochemical dissection of the S. pennellii acylglucose biosynthetic pathway identified a trichome gland cell expressed invertase-like enzyme that hydrolyzes acylsucroses (Sopen03g040490). This enzyme acts on the pyranose ring-acylated acylsucroses found in the wild tomato but not the furanose ring-decorated acylsucroses of cultivated tomato. These results show that modification of the core acylsucrose biosynthetic pathway leading to loss of furanose ring acylation set the stage for co-option of a general metabolic enzyme to produce a new class of protective compounds.