Modern approaches to study plant–insect interactions in chemical ecology

Dyer, Lee A.; Philbin, Casey S.; Ochsenrider, Kaitlin M.; Richards, Lora A.; Massad, Tara Joy; Smilanich, Angela M.; Forister, Matthew L.; Parchman, Thomas L.; Galland, Lanie M.; Hurtado, Paul J.; Espeset, Anne; Glassmire, Andrea E.; Harrison, Joshua G.; Mo, Carmen; Yoon, Su’ad A.; Pardikes, Nicholas A.; Muchoney, Nadya D.; Jahner, Joshua P.; Slinn, Heather L.; Shelef, Oren; Dodson, Craig D.; Kato, Massuo Jorge; Yamaguchi, Lydia F.; Jeffrey, Christopher S.

doi:10.1038/s41570-018-0009-7

Cited by 97 publications

(96 citation statements)

References 177 publications

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“…Structurally diverse specialized metabolites are central players in plants’ adaptations to their environments and in particular in their defense against enemies ( 1 ). The spectacular diversification of specialized metabolism found in plants inspired several decades of intense research about its multifaceted ecological functions and nucleated a long list of plant defense theories that provided important guidance to empirical studies of the evolution and ecology of plant-insect interactions ( 2 ). However, these plant defense theories did not follow the canonical path of hypothetical-deductive reasoning in which critical predictions are posed at the same levels of analysis ( 3 ) and tested experimentally to advance the next cycle of theory development ( 4 ).…”

Section: Introductionmentioning

confidence: 99%

Information theory tests critical predictions of plant defense theory for specialized metabolism

Halitschke

Baldwin

et al. 2020

Preprint

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1Different plant defense theories have provided important theoretical guidance in 2 explaining patterns in plant specialized metabolism, but their critical predictions remain to be 3 tested. Here, we systematically explored the metabolomes of Nicotiana attenuata, from single 4 plants to populations, as well as of closely-related species, using unbiased MS/MS analyses and 5 processed the abundances of compound-spectrum-based MS features within an information 6 theory framework to test critical predictions of Optimal Defense (OD) and Moving Target (MT) 7 theories. Information components of herbivory-elicited plant metabolomes were fully consistent 8 with the OD theory predictions and contradicted the main prediction of the MT theory. From 9 micro-to macro-evolutionary scales, jasmonate signaling was identified as the master 10 determinant of OD while ethylene signaling provided fine-tuning for herbivore-specific responses 11 annotated via MS/MS molecular networks. 12Plant defense theory, Information theory. 14 15 One-sentence summary: Information theory tests defense theory predictions by providing a 16 common currency for comparison of specialized metabolomes 17 Introduction 1 Structurally diverse specialized metabolites are central players in plants' adaptations to 2 their environments and in particular in their defense against enemies (1). The spectacular 3 diversification of specialized metabolism found in plants inspired several decades of intense 4 research about its multifaceted ecological functions and nucleated a long list of plant defense 5 theories that provided important guidance to empirical studies of the evolution and ecology of 6 plant-insect interactions (2). However, these plant defense theories did not follow the canonical 7 path of hypothetical-deductive reasoning in which critical predictions are posed at the same levels 8 of analysis (3) and tested experimentally to advance the next cycle of theory development (4).9Technical constraints limited data acquisition to specific metabolic classes and precluded the 10 comprehensive profiling of specialized metabolites and consequently, prevented the among-taxa 11 comparisons which were essential for theory advancement (5). This lack of comprehensive 12 metabolomics data and the processing workflows to compare the metabolic space among 13 different plant taxa in a common currency thwarted the scientific maturation of the field. 14 Recent advances in the field of tandem mass spectrometry (MS/MS) metabolomics are 15 allowing for comprehensive and high-throughput characterizations of metabolic variations within 16 and among species that comprise complete phylogenetic clades particularly when computational 17 methods are employed for the calculation of structural similarity among complex mixtures 18 without a priori chemical knowledge (5). This combination of analytical and computational 19advances provides the missing framework required for the rigorous testing of many predictions 20 made by the long-standing ecological and evolutionary theories on metab...

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Section: Introductionmentioning

confidence: 99%

Information theory tests critical predictions of plant defense theory for specialized metabolism

Halitschke

Baldwin

et al. 2020

Preprint

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“…In most cases, progress has been made by chemical ecologists focusing on small subsets of the secondary metabolites produced by plants and consumed by herbivores. The focus on a few charismatic molecules or classes of compounds, such as furanocoumarins (Berenbaum, 1983) or cardiac glycosides (Zalucki et al , 2001), was at least in part necessitated by early methods in natural products chemistry that were targeted and not easily optimized for the discovery of large suites of co-occurring primary and secondary metabolites (Maag et al , 2015; Dyer et al , 2018). As technological limitations have dissipated, the opportunity now exists for a deeper understanding of the challenges faced by herbivores, with the possibility of discovering, among other things, novel compounds and synergistic interactions among compounds (Prince & Pohnert, 2010; Richards et al , 2010; Sardans et al , 2011).…”

Section: Introductionmentioning

confidence: 99%

Caterpillars on a phytochemical landscape: the case of alfalfa and the Melissa blue butterfly

Forister

Yoon

Philbin

et al. 2018

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25 26 42 including alkaloids, phenolic glycosides and saponins. The saponins are represented in our data 43 by more than 25 individual compounds with beneficial and detrimental effects on caterpillars, 44 which highlights the value of metabolomic data as opposed to approaches that rely on total 45 concentrations within defensive classes. 46 47 48 49 50 51 52One of the conceptual pillars of trophic ecology is the idea that herbivores must overcome the 53 barrier of plant secondary chemistry before extracting the nutrients necessary for growth and 54 reproduction (Feeny et al., 1992). The success of this idea is reflected in areas of research that 55 include coevolution (Agrawal et al., 2012), ecological specialization (Dyer, 1995), and nutrient 56 flow in ecosystems (Olson, 1963). In most cases, progress has been made by chemical ecologists 57 focusing on small subsets of the secondary metabolites produced by plants and consumed by 58 herbivores. The focus on a few charismatic molecules or classes of compounds, such as 59 furanocoumarins (Berenbaum, 1983) or cardiac glycosides (Zalucki et al., 2001), was at least in 60 part necessitated by early methods in natural products chemistry that were targeted and not easily 61 optimized for the discovery of large suites of co-occurring primary and secondary metabolites 62 (Maag et al., 2015; Dyer et al., 2018). As technological limitations have dissipated, the 63 opportunity now exists for a deeper understanding of the challenges faced by herbivores, with 64 the possibility of discovering, among other things, novel compounds and synergistic interactions 65 among compounds (Prince & Pohnert, 2010; Richards et al., 2010; Sardans et al., 2011). More 66 generally, an important task is to quantify the phytochemical dimensionality of the antagonistic 67 interaction between plants and herbivores, with an eye towards understanding constraints on the 68 evolution of both players (Fordyce & Nice, 2008; Macel et al., 2010) and predicting the 69 formation of new plant-herbivore interactions (Erbilgin, 2018). Here we use the example of a 70 specialized herbivore and a novel host plant to investigate the phytochemical landscape from the 71 perspective of developing caterpillars. 72 The Melissa blue butterfly, Lycaeides melissa, specializes on larval host plants in the pea 73 family (Fabaceae), primarily in the genera Astragalus and Lupinus. Within the last 200 years, L. 74 melissa has colonized introduced alfalfa, Medicago sativa (Fabaceae), at least twice and 75 probably multiple times (Chaturvedi et al., 2018), forming a heterogeneous patchwork of 76 association throughout the range of the butterfly in western North America. M. sativa is a 77 suboptimal host, relative to native hosts that have been examined, and populations of the 78 butterfly that persist on M. sativa show evidence of loss of preference for native hosts (Forister et 79 al., 2012), reduced caterpillar performance on native hosts, and a slight increase in ability to 80 develop on the suboptimal novel host (Gompert et...

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“…Reductionist approaches in focal systems have revealed key aspects of host recognition ( 3 ) and other relevant mechanisms ( 4 ), but by design do not encompass context dependence including interacting species and abiotic variation. Ecological studies of host range, in contrast, might quantify context dependence but have not always included modern genomic and metabolomic approaches ( 5 ). Here we use the colonization of alfalfa, Medicago sativa , by the Melissa blue butterfly , Lycaeides melissa (Fig.…”

Section: Main Textmentioning

confidence: 99%

Leveraging biological complexity to predict patch occupancy in a recent host range expansion

Forister

Philbin

Marion

et al. 2020

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30Specialized plant-insect interactions are a defining feature of life on earth, yet we are only 31 beginning to understand the factors that set limits on host ranges in herbivorous insects. To 32 understand the colonization of alfalfa by the Melissa blue butterfly, we quantified arthropod 33 assemblages and plant metabolites across a wide geographic region, while controlling for climate 34 and dispersal inferred from population genomic variation. The presence of the butterfly is 35 successfully predicted by direct and indirect effects of plant traits and interactions with other 36 species. Results are consistent with the predictions of a theoretical model of parasite host range 37 in which specialization is an epiphenomenon of the many barriers to be overcome rather than a 38 consequence of trade-offs in developmental physiology. 39 40 One sentence summary: 41 The formation of a novel plant-insect interaction can be predicted with a combination of biotic 42 and abiotic factors, with comparable importance revealed for metabolomic variation in plants 43 and interactions with mutualists, competitors and enemies. 44 45 p.3 46 Main text: 47 129generalist herbivores or parasites (with many accumulated hosts) are predictably rare across 130 geographic and phylogenetic scales (29, 30). The complexity of barriers to novel host use and 131 the ecological contingency of colonization challenge our ability to forecast new crop pests or 132 emerging infectious diseases (1), but the multi-disciplinary approach illustrated here does raise 133 the promise, at least for herbivorous insects, that expansions of host range can be understood 134 given current technologies and sufficient sampling effort. 135 136 137 157 the ecological trap hypothesis. Oecologia. 181, 985-996 (2016).158 10. Z. Gompert et al., Admixture and the organization of genetic diversity in a butterfly 159 species complex revealed through common and rare genetic variants. Mol. Ecol. 23, 4555-160 p.8 4573 (2014). 161 11. M. L. Forister, C. C. Nice, J. A. Fordyce, Z. Gompert, Host range evolution is not driven 162 by the optimization of larval performance: the case of Lycaeides melissa (Lepidoptera: 163 Lycaenidae) and the colonization of alfalfa.

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Modern approaches to study plant–insect interactions in chemical ecology

Cited by 97 publications

References 177 publications

Information theory tests critical predictions of plant defense theory for specialized metabolism

Information theory tests critical predictions of plant defense theory for specialized metabolism

Caterpillars on a phytochemical landscape: the case of alfalfa and the Melissa blue butterfly

Leveraging biological complexity to predict patch occupancy in a recent host range expansion

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