Ecological interactions affect the bioactivity of medicinal plants

Abstract

Essential oils produced by medicinal plants possess important bioactive properties (antibacterial, antioxidant) of high value for human society. Pollination and herbivory can modify the chemical defences of plants and therefore they may influence the bioactivity of essential oils. However, the effect of ecological interactions on plant bioactivity has not yet been evaluated. We tested the hypothesis that cross-pollination and simulated herbivory modify the chemical composition of essential oils, improving the bioactive properties of the medicinal plant Lepechinia floribunda (Lamiaceae). Through controlled experiments, we showed that essential oils from the outcrossed plant progeny had a higher relative abundance of oxygenated terpenes and it almost doubled the bacteriostatic effect on Staphylococcus aureus, compared to inbred progeny (i.e., progeny produced in absence of pollinators). Herbivory affected negatively and positively the production of rare compounds in inbred and outcrossed plants, respectively, but its effects on bioactivity still remain unknown. We show for the first time that by mediating cross-pollination (indirect ecosystem service), pollinators can improve ecosystem services linked to the biological activity of plant's essential oils. We stress the importance of the qualitative component of pollination (self, cross); an aspect usually neglected in studies of pollination services.

Figure 1

Graphical hypothesis: Cross-pollination and herbivory improve bioactive properties of plants against microorganisms. It is expected that outcrossed plant progeny (left side) have higher bioactive essential oils than inbred plant progeny (absence of pollinators, right side). It is also expected that herbivory increases bioactivity but in higher magnitude in outcrossed plant progeny. Icons used in this figure are from the Noun Project (https://thenounproject.com).

Figure 2

Heatmap showing the relative abundance of the 25 chemical compounds of the essential oil of Lepechinia floribunda. Pollination and simulated herbivory treatments, IwH: inbred plants without simulated herbivory, IH: inbred plants with simulated herbivory, OwH: outcrossed plants without simulated herbivory, OH: outcrossed plants with simulated herbivory. Compounds are ordered according to their frequency of occurrence among the tested plants: priority (present in 100% of plants), non-priority (present in less than 100% and more than 30% of plants) and rare compounds (present in less than 30% of plants). Colors shown in the upright scale represent the relative abundances of compounds (i.e., the percentage of × compound in the essential oil of a plant) from more than zero to 60%, and white cells show absence of compounds. Each row represents an individual plant, and each column represents a chemical compound (signaled with letters) a: borneol, b: β caryophyllene, c: aromadendrene, d: α humulene, e: ledol plus unidentified oxygenated sesquiterpene compound, probably a precursor of ledol, f: α terpineol, g: bornyl acetate, h: α gurjunene, i: 1,8 cineol, j: alloaromadendrene, k: α amorphene, l: ledene, m: α fernesene, n: β selinene, o: nerolidol, p: palustrol, q: tau cadinol, r: α bulnesene, s: α pinene, t: camphene, u: β pinene, v: β gurjunene, w: α guaiene, x: γ cadinene, y: α eudesmol. The R software (function pheatmap of the library “pheatmap”, version 4.1.2) was used to create this heatmap.

Figure 3

Mean (± SD) relative abundance of the four terpene groups present in the essential oil of Lepechinia floribunda (hydrocarbon monoterpenes, oxygenated monoterpenes, hydrocarbon sesquiterpenes and oxygenated sesquiterpenes) expressed as indices. (a): T index = ln (relative abundance of monoterpenes/relative abundance of sesquiterpenes). (b): M index = ln (relative abundance of hydrocarbon monoterpenes/relative abundance of oxygenated monoterpenes), and c: S index = ln (relative abundance of hydrocarbon sesquiterpenes/relative abundance of oxygenated sesquiterpenes). Abbreviations, OP outcrossed plants, IP inbred plants. Simulated herbivory (red), without simulated herbivory (blue).