Toxicity of Milkweed Leaves and Latex: Chromatographic Quantification Versus Biological Activity of Cardenolides in 16 Asclepias Species

Züst, Tobias; Petschenka, Georg; Hastings, Amy P.; Agrawal, Anurag A. (2019). Toxicity of Milkweed Leaves and Latex: Chromatographic Quantification Versus Biological Activity of Cardenolides in 16 Asclepias Species. Journal of Chemical Ecology, 45(1), pp. 50-60. Springer 10.1007/s10886-018-1040-3

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Cardenolides are classically studied steroidal defenses in chemical ecology and plant-herbivore coevolution. Although milkweed plants (Asclepias spp.) produce up to 200 structurally different cardenolides, all compounds seemingly share the same well-characterized mode of action, inhibition of the ubiquitous Na+/K+ ATPase in animal cells. Over their evolutionary radiation, milkweeds show a quantitative decline of cardenolide production and diversity. This reduction is contrary to coevolutionary predictions and could represent a cost-saving strategy, i.e. production of fewer but more toxic cardenolides. Here we test this hypothesis by tandem cardenolide quantification using HPLC (UV absorption of the unsaturated lactone) and a pharmacological assay (in vitro inhibition of a sensitive Na+/K+ ATPase) in a comparative study of 16 species of Asclepias. We contrast cardenolide concentrations in leaf tissue to the subset of cardenolides present in exuding latex. Results from the two quantification methods were strongly correlated, but the enzymatic assay revealed that milkweed cardenolide mixtures often cause stronger inhibition than equal amounts of a non-milkweed reference cardenolide, ouabain. Cardenolide concentrations in latex and leaves were positively correlated across species, yet latex caused 27% stronger enzyme inhibition than equimolar amounts of leaf cardenolides. Using a novel multiple regression approach, we found three highly potent cardenolides (identified as calactin, calotropin, and voruscharin) to be primarily responsible for the increased pharmacological activity of milkweed cardenolide mixtures. However, contrary to an expected trade-off between concentration and toxicity, later-diverging milkweeds had the lowest amounts of these potent cardenolides, perhaps indicating an evolutionary response to milkweed’s diverse community of specialist cardenolide-sequestering insect herbivores.

Item Type:

Journal Article (Original Article)

Division/Institute:

08 Faculty of Science > Department of Biology > Institute of Plant Sciences (IPS) > Biotic Interactions
08 Faculty of Science > Department of Biology > Institute of Plant Sciences (IPS)

UniBE Contributor:

Züst, Tobias

Subjects:

500 Science > 580 Plants (Botany)

ISSN:

0098-0331

Publisher:

Springer

Language:

English

Submitter:

Peter Alfred von Ballmoos-Haas

Date Deposited:

05 Feb 2019 12:35

Last Modified:

23 Oct 2019 00:38

Publisher DOI:

10.1007/s10886-018-1040-3

Related URLs:

PubMed ID:

30523520

Uncontrolled Keywords:

cardiac glycoside; coevolution; macroevolutionary escalation; mode of action; monarch butterfly; na+/k+ atpase; phylogenetic chemical ecology; plant-insect interactions; structure-activity relationships; target site insensitivity

BORIS DOI:

10.7892/boris.122688

URI:

https://boris.unibe.ch/id/eprint/122688

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