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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 adultDrosophila melanogasterwith 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.
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Consequences and Costs of Chemical Complexity: The Evolutionary Ecology of Direct Phytochemical Defense against Herbivores
Phytochemical defenses, plant-produced compounds that can deter or slow herbivores, are critical in influencing the interactions between herbivores and their host plants—some of the most diverse and abundant organisms on earth. We discuss the foundational findings and theories related to the direct defense of plants against herbivores by these compounds, as well as continuing research questions in this field. We highlight the costs associated with phytochemical defense production and variation within individual plants in the distribution of phytochemicals, both spatially and temporally. We then discuss coevolutionary theory and the adaptations of herbivores to cope with phytochemical defense compounds. Last, we delve into the incredible diversity of phytochemical compounds, the role of diversity in herbivory, and new ways of measuring and understanding phytochemical diversity.
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- Award ID(s):
- 1855927
- PAR ID:
- 10514951
- Publisher / Repository:
- The University of Chicago Press
- Date Published:
- Journal Name:
- International Journal of Plant Sciences
- Volume:
- 185
- Issue:
- 1
- ISSN:
- 1058-5893
- Page Range / eLocation ID:
- 3 to 14
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract As a general rule, plants defend against herbivores with multiple traits. The defense synergy hypothesis posits that some traits are more effective when co‐expressed with others compared to their independent efficacy. However, this hypothesis has rarely been tested outside of phytochemical mixtures, and seldom under field conditions. We tested for synergies between multiple defense traits of common milkweed (Asclepias syriaca) by assaying the performance of two specialist chewing herbivores on plants in natural populations. We employed regression and a novel application of random forests to identify synergies and antagonisms between defense traits. We found the first direct empirical evidence for two previously hypothesized defense synergies in milkweed (latex by secondary metabolites, latex by trichomes) and identified numerous other potential synergies and antagonisms. Our strongest evidence for a defense synergy was between leaf mass per area and low nitrogen content; given that these “leaf economic” traits typically covary in milkweed, a defense synergy could reinforce their co‐expression. We report that each of the plant defense traits showed context‐dependent effects on herbivores, and increased trait expression could well be beneficial to herbivores for some ranges of observed expression. The novel methods and findings presented here complement more mechanistic approaches to the study of plant defense diversity and provide some of the best evidence to date that multiple classes of plant defense synergize in their impact on insects. Plant defense synergies against highly specialized herbivores, as shown here, are consistent with ongoing reciprocal evolution between these antagonists.more » « less
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Interactions between plants and leaf herbivores have long been implicated as the major driver of plant secondary metabolite diversity. However, other plant-animal interactions, such as those between fruits and frugivores, may also be involved in phytochemical diversification. Using 12 species of Piper , we conducted untargeted metabolomics and molecular networking with extracts of fruits and leaves. We evaluated organ-specific secondary metabolite composition and compared multiple dimensions of phytochemical diversity across organs, including richness, structural complexity, and variability across samples at multiple scales within and across species. Plant organ identity, species identity, and the interaction between the two all significantly influenced secondary metabolite composition. Leaves and fruit shared a majority of compounds, but fruits contained more unique compounds and had higher total estimated chemical richness. While the relative levels of chemical richness and structural complexity across organs varied substantially across species, fruit diversity exceeded leaf diversity in more species than the reverse. Furthermore, the variance in chemical composition across samples was higher for fruits than leaves. By documenting a broad pattern of high phytochemical diversity in fruits relative to leaves, this study lays groundwork for incorporating fruit into a comprehensive and integrative understanding of the ecological and evolutionary factors shaping secondary metabolite composition at the whole-plant level.more » « less
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Glucosinolates are an important class of secondary metabolites in Brassicales plants with a critical role in chemical defense. Glucosinolates are chemically inactive but can be hydrolyzed by myrosinases to produce a range of chemically active compounds toxic to herbivores and pathogens, thereby constituting the glucosinolate–myrosinase defense system or the mustard oil bomb. During the evolution, Brassicales plants have developed not only complex biosynthetic pathways for production of a large number of glucosinolate structures but also different classes of myrosinases that differ in catalytic mechanisms and substrate specificity. Studies over the past several decades have made important progress in the understanding of the cellular and subcellular organization of the glucosinolate–myrosinase system for rapid and timely detonation of the mustard oil bomb upon tissue damage after herbivore feeding and pathogen infection. Progress has also been made in understanding the mechanisms that herbivores and pathogens have evolved to counter the mustard oil bomb. In this review, we summarize our current understanding of the function and organization of the glucosinolate–myrosinase system in Brassicales plants and discuss both the progresses and future challenges in addressing this complex defense system as an excellent model for analyzing plant chemical defense.more » « less
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{"Abstract":["Original data and R code to accompany the manuscript: "Interaction diversity explains the maintenance of phytochemical diversity" by Susan R. Whitehead, Ethan Bass, Alexsandra Corrigan, André Kessler, and Katja Poveda Accepted for publication in Ecology Letters<\/p>\n\nAbstract: The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer-specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.<\/p>\n\nhttps://github.com/WhiteheadLabVT/Phytochemical-Diversity-Experiment/releases/tag/v1.0.0<\/p>"]}more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1086/727902
