Relative Selectivity of Plant Cardenolides for Na+/K+-ATPases From the Monarch Butterfly and Non-resistant Insects.

Georg Petschenka,Juan J Araya,Anurag A Agrawal,Barbara N Timmermann,Susanne Schröder,Colleen S Fei

doi:10.3389/fpls.2018.01424

Abstract

A major prediction of coevolutionary theory is that plants may target particular herbivores with secondary compounds that are selectively defensive. The highly specialized monarch butterfly (Danaus plexippus) copes well with cardiac glycosides (inhibitors of animal Na+/K+-ATPases) from its milkweed host plants, but selective inhibition of its Na+/K+-ATPase by different compounds has not been previously tested. We applied 17 cardiac glycosides to the D. plexippus-Na+/K+-ATPase and to the more susceptible Na+/K+-ATPases of two non-adapted insects (Euploea core and Schistocerca gregaria). Structural features (e.g., sugar residues) predicted in vitro inhibitory activity and comparison of insect Na+/K+-ATPases revealed that the monarch has evolved a highly resistant enzyme overall. Nonetheless, we found evidence for relative selectivity of individual cardiac glycosides reaching from 4- to 94-fold differences of inhibition between non-adapted Na+/K+-ATPase and D. plexippus-Na+/K+-ATPase. This toxin receptor specificity suggests a mechanism how plants could target herbivores selectively and thus provides a strong basis for pairwise coevolutionary interactions between plants and herbivorous insects.

Highlights

It is widely recognized that coevolution between plants and herbivores occurs in a community context (Agrawal, 2005; Johnson and Stinchcombe, 2007; Poelman and Kessler, 2016), but the mechanisms and consequences of such complex interactions are unclear
To test the prediction that structurally diverse compounds exert differential pharmacological activities and may target different herbivore species selectively, here we report on studies where we applied 16 different cardenolides and one bufadienolide to the Na+/K+-ATPase of the monarch butterfly, a closely related basal milkweed butterfly Euploea core, as well as to the Na+/K+ATPase of an insect not adapted to dietary cardiac glycosides
While the D. plexippus-Na+/K+-ATPase is consistently more resistant than the non-adapted insect Na+/K+-ATPases of E. core and S. gregaria (Figure 2 and Supplementary Table S1), 11 out of 16 cardenolides tested acted stronger on its Na+/K+ATPase than ouabain

Summary

Introduction

It is widely recognized that coevolution between plants and herbivores occurs in a community context (Agrawal, 2005; Johnson and Stinchcombe, 2007; Poelman and Kessler, 2016), but the mechanisms and consequences of such complex interactions are unclear. Coevolutionary studies have found some evidence that different herbivores can select for specific defensive traits (Mithen et al, 1995; Züst et al, 2012; Castillo et al, 2014) and it was demonstrated that selective interactions between plant defensive compounds and herbivores exist, i.e., that the same substance can have different effects on different herbivores (Ayres et al, 1997; Linhart and Thompson, 1999). As a first step to address the potential for coevolution between species at the interface of toxins and receptors, one must demonstrate that individual toxins act selectively on targets from different species, i.e., a specific plant toxin is affecting one herbivore’s physiological target relatively stronger or weaker compared to that of another herbivore species

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Conclusion