Abstract Premise The specialized metabolites of plants are recognized as key chemical traits in mediating the ecology and evolution of sundry plant–biotic interactions, from pollination to seed predation. Intra‐ and interspecific patterns of specialized metabolite diversity have been studied extensively in leaves, but the diverse biotic interactions that contribute to specialized metabolite diversity encompass all plant organs. Focusing on two species of Psychotria shrubs, we investigated and compared patterns of specialized metabolite diversity in leaves and fruit with respect to each organ's diversity of biotic interactions. Methods To evaluate associations between biotic interaction diversity and specialized metabolite diversity, we combined UPLC‐MS metabolomic analysis of foliar and fruit specialized metabolites with existing surveys of leaf‐ and fruit‐centered biotic interactions. We compared patterns of specialized metabolite richness and variance among vegetative and reproductive tissues, among plants, and between species. Results In our study system, leaves interact with a far larger number of consumer species than do fruit, while fruit‐centric interactions are more ecologically diverse in that they involve antagonistic and mutualistic consumers. This aspect of fruit‐centric interactions was reflected in specialized metabolite richness—leaves contained more than fruit, while each organ contained over 200 organ‐specific specialized metabolites. Within each species, leaf‐ and fruit‐specialized metabolite composition varied independently of one another across individual plants. Contrasts in specialized metabolite composition were stronger between organs than between species. Conclusions As ecologically disparate plant organs with organ‐specific specialized metabolite traits, leaves and fruit can each contribute to the tremendous overall diversity of plant specialized metabolites.
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Comparative Metabolomics of Fruits and Leaves in a Hyperdiverse Lineage Suggests Fruits Are a Key Incubator of Phytochemical Diversification
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.
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- Award ID(s):
- 1856776
- PAR ID:
- 10338754
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 12
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Phytochemical diversity is an effective plant defensive attribute, but much more research has focused on genetic and environmental controls of specific defensive compounds than phytochemical diversity
per se . Documenting plasticity in phytochemical richness and plant chemical composition as opposed to individual compounds is important for understanding plant defense. This study outlines a multi-site transplant experiment in Cerrado gallery forests in central Brazil, utilizingPiper arboreum (Piperaceae), a prevalent and widespread neotropical shrub. Clones from four distinct populations were planted either at their origin site or in a different forest. Secondary metabolite composition varied between populations initially and then changed after transplanting. Interestingly, clones with chemical profiles that were distinct from the populations where they were introduced experienced reduced specialist chrysomelid herbivory compared to clones that were more chemically similar to the existingP. arboreum populations where they were planted. Specialist Lepidoptera herbivory also declined in clones transplanted to a new forest, but this change could not be ascribed to chemical profiles. In contrast, generalist herbivory was unaffected by chemical dissimilarity and transplanting. This research adds to the expanding body of evidence suggesting that phytochemical diversity is a dynamic trait exerting unique effects on different herbivore guilds. -
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Abstract Species richness in tropical forests is correlated with other dimensions of diversity, including the diversity of plant–herbivore interactions and the phytochemical diversity that influences those interactions. Understanding the complexity of plant chemistry and the importance of phytochemical diversity for plant–insect interactions and overall forest richness has been enhanced significantly by the application of metabolomics to natural systems. The present work used proton nuclear magnetic resonance spectroscopy (1H‐NMR) profiling of crude leaf extracts to study phytochemical similarity and diversity among
Piper plants growing naturally in the Atlantic Rainforest of Brazil. Spectral profile similarity and chemical diversity were quantified to examine the relationship between metrics of phytochemical diversity, specialist and generalist herbivory, and understory plant richness. Herbivory increased with understory species richness, while generalist herbivory increased and specialist herbivory decreased with the diversity ofPiper leaf material available. Specialist herbivory increased when conspecific host plants were more spectroscopically dissimilar. Spectral similarity was lower among individuals of common species, and they were also more spectrally diverse, indicating phytochemical diversity is beneficial to plants. Canopy openness and soil nutrients also influenced chemistry and herbivory. The complex relationships uncovered in this study add information to our growing understanding of the importance of phytochemical diversity for plant–insect interactions and tropical plant species richness. -
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Abstract 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 a set of 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.
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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
Abstract: 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.
https://github.com/WhiteheadLabVT/Phytochemical-Diversity-Experiment/releases/tag/v1.0.0
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2021.693739
