Plant chemical diversity enhances defense against herbivory

• 成果类型: Article
• 署名作者: Lopez-Goldar, Xose; Zhang, Xuening; Hastings, Amy P.; Duplais, Christophe; Agrawal, Anurag A.
• 署名单位: Cornell University; Cornell University; Cornell University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-12523
• DOI: 10.1073/pnas.2417524121
• 发表日期: 2024-12-09
• 关键词: layer-chromatography profiles; danaus-plexippus lepidoptera; phytochemical diversity; monarch butterflies; cardenolide content; emetic potency; danaidae; apocynales; milkweed

摘要

Multiple hypotheses have been put forth to understand why defense chemistry in individual plants is so diverse. A major challenge has been teasing apart the importance of concentration vs. composition of defense compounds and resolving the mechanisms of diversity effects that determine plant resistance against herbivores. Accordingly, we first outline nonexclusive mechanisms by which phytochemical diversity may increase toxicity of a mixture compared to the average effect of each compound alone. We then leveraged independent in vitro, in vivo transgenic, and organismal experiments to test the effect of equimolar concentrations of purified milkweed toxins in isolation vs. mixtures on the specialist and sequestering monarch butterfly. We show that cardenolide toxin mixtures from milkweed plants enhance resistance against this herbivore compared to equal concentrations of single compounds. In mixtures, highly potent toxins dominated the inhibition of the monarch's target enzyme (Na+/K+- ATPase) in vitro, revealing toxin- specific affinity for the adapted enzyme in the absence of other physiological adaptations of the monarch. Mixtures also caused increased mortality in CRISPR- edited adult Drosophila melanogaster with the monarch enzyme in vivo, whereas wild- type flies showed lower survival regardless of mixture type. Finally, although experimentally administered mixtures were not more toxic to monarch caterpillars than single compounds overall, increasing caterpillar sequestration from mixtures resulted in an increasing burden for growth compared to single compounds. Phytochemical diversity likely provides an economical plant defense by acting on multiple aspects of herbivore physiology and may be particularly effective against sequestering specialist herbivores.