Traditional medicinal use is linked with apparency, not specialized metabolite profiles in the order Caryophyllales

Abstract

A better understanding of the relationship between plant specialized metabolism and traditional medicinal use has the potential to aid in bioprospecting and the untangling of cross-cultural plant use patterns. However, given the limited information available for metabolites in most plant species, associating medicinal properties with a metabolite can be difficult. The order Caryophyllales has a unique pattern of lineages of tyrosine- or phenylalanine-dominant specialized metabolism, represented by mutually exclusive anthocyanin and betalain pigments, making the group ideal to work around a lack of detailed knowledge of specific metabolites. We compiled a list of medicinal species in selected tyrosine- or phenylalanine-dominant families of Caryophyllales across the globe (Nepenthaceae, Polygonaceae, Simmondsiaceae, Microteaceae, Caryophyllaceae, Amaranthaceae, Limeaceae, Molluginaceae, Portulacaceae, Cactaceae, and Nyctaginaceae) by searching scientific literature until no new uses were recovered, and tested for phylogenetic clustering of medicinal uses using a "hot nodes" approach. To test potential non-metabolite drivers of medicinal use, like how often humans encounter a species (apparency), we repeated the same analysis in North American species across the entire order and performed phylogenetic generalized least squares regression (PGLS) with occurrence data from the Global Biodiversity Information Facility (GBIF). We hypothesized families with Tyr-enriched metabolism would show clustering of different types of medicinal use compared to the ancestral Phe-enriched metabolism. Instead, weedy, wide-ranging clades in Polygonaceae and Amaranthaceae are overrepresented across nearly all types of medicinal use. Therefore, we found that apparency is a better predictor of medicinal use than metabolite profiles, although metabolism type may still be a contributing factor.