Abstract
Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity.
Highlights
Despite the enormous structural diversity of plant specialized metabolites, they are derived from a relatively small number of primary metabolites, such as sugars, amino acids, nucleotides, and fatty acids (Maeda, 2019)
Because tomato acylsucrose biosynthesis occurs in trichomes, candidate genes in this region were filtered based on their trichome-specific expression patterns
This study identified a S. lycopersicum chromosome 7 synteny of ACS, ECH, and BAHD acyltransferase genes including two involved in medium chain acylsugar biosynthesis
Summary
Despite the enormous structural diversity of plant specialized metabolites, they are derived from a relatively small number of primary metabolites, such as sugars, amino acids, nucleotides, and fatty acids (Maeda, 2019). The experiments identified two genes known as AACS and AECH in tomatoes that produce acylsugars with long chains These two genes originated from the genes of older enzymes that metabolize fatty acids – the building blocks of fats – in plant cells. This revealed that AACS and AECH emerged in the nightshade family around the same time that longer chains of acylsugars started appearing These findings provide insights into how plants evolved to be able to produce a variety of secondary metabolites that may protect them from a broader range of pests. These results provide insights into specialized metabolic evolution through emergence of cell-type specific gene expression, the formation of metabolic gene clusters and illuminates additional examples of primary metabolic enzymes being co-opted into specialized metabolism
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