Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

Abstract

The coexpression of plant resistance traits suggests the hypothesis that they may have complementary functions in defense against herbivory. To address the extent to which defensive traits are necessarily coupled in plants grown under various conditions, we focused on latex and cardenolides, two potent defenses of milkweeds. We measured defenses across ontogenetic stages, different biotic and abiotic environments, and across genetic families of the common milkweed Asclepias syriaca. We first addressed the extent to which foliar cardenolides are derived from latex because latex actively flows through canals in leaves. We rinsed latex out of shredded leaves, which had no impact on foliar cardenolides, suggesting cardenolides are allocated to leaves independently of latex. Accordingly, there is potential for independent expression of the two traits. We next followed a cohort of plants from germination over three years; expression of both latex exudation and cardenolides increased annually, with the exception of a second year dip in cardenolides. Damage by monarch caterpillars induced ≈50% increases of both latex and cardenolides, with the former occurring rapidly within a day and the latter taking five days of herbivory; these responses were preceded by an earlier peak of the signaling hormones jasmonic acid and abscisic acid. Endogenous jasmonic acid showed an instantaneous positive correlation with latex exudation and foliar cardenolides. Under drought stress, latex and cardenolide expression were reversed, with water stress suppressing latex exudation, but nearly doubling cardenolide concentrations. These drought effects were not driven by phytohormones in the expected manner, as jasmonic acid was unaffected, salicylic acid was strongly suppressed, and abscisic acid tripled in response to drought. Finally, a meta‐analysis of four previously published field studies representing 85 genetic families of A. syriaca revealed no evidence for a genetic correlation between latex exudation and foliar cardenolide concentrations. The same lack of a correlation was observed across 22 populations of A. syriaca when grown in a common environment. Thus, the two most important defensive traits of milkweeds, although often coexpressed, can become uncoupled during some ontogenetic stages, under some biotic and abiotic conditions, and there is no evidence that they evolve together.