Compartmentalization of specialized metabolites across vegetative and reproductive tissues in two sympatric Psychotria species

Abstract

Premise: The specialized metabolites of plants are recognized as key chemical traits in mediating the ecology and evolution of sundry plant-biotic interactions, from pollination to seed predation. Intra-and interspecific patterns of specialized metabolite diversity have been studied extensively in leaves, but the diverse biotic interactions that contribute to specialized metabolite diversity encompass all plant organs. Focusing on two species of Psychotria shrubs, we investigated and compared patterns of specialized metabolite diversity in leaves and fruit with respect to each organ's diversity of biotic interactions. Methods: To evaluate associations between biotic interaction diversity and specialized metabolite diversity, we combined UPLC-MS metabolomic analysis of foliar and fruit specialized metabolites with existing surveys of leaf-and fruit-centered biotic interactions. We compared patterns of specialized metabolite richness and variance among vegetative and reproductive tissues, among plants, and between species. Results: In our study system, leaves interact with a far larger number of consumer species than do fruit, while fruit-centric interactions are more ecologically diverse in that they involve antagonistic and mutualistic consumers. This aspect of fruit-centric interactions was reflected in specialized metabolite richness-leaves contained more than fruit, while each organ contained over 200 organ-specific specialized metabolites. Within each species, leaf-and fruit-specialized metabolite composition varied independently of one another across individual plants. Contrasts in specialized metabolite composition were stronger between organs than between species. Conclusions: As ecologically disparate plant organs with organ-specific specialized metabolite traits, leaves and fruit can each contribute to the tremendous overall diversity of plant specialized metabolites.