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

Abstract

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...

Ethylene is a local modulator of jasmonate‐dependent phenolamide accumulation during Manduca sexta herbivory in Nicotiana attenuata

“…It was identified that, while JA is the central signal shaping the amplitude of convergent metabolic responses to both herbivories, ET fine-tunes the specificity of this metabolic response according to the herbivore diet breadth. The latter study, as in the present one, detected that phenolamides are the foliar metabolites whose production is most tightly dependent on the fine-tuning signaling function of ET (Li et al 2020). This convergence further reinforces a role of ET in mitigating the production of these metabolites according to insect herbivory type and echoes ecological implications suggested for the well-known function of ET in antagonizing the JA-dependent accumulation of nicotine when tobacco plants are attacked by nicotine-tolerant M. sexta larvae.…”

“…In a recent large-scale metabolomics study, the degree of plasticity and diversity of the specialized metabolic profile of different Nicotiana species was investigated in response to herbivory by a "specialist" (M. sexta) and a "generalist" (Spodoptera littoralis, the cotton leaf worm) chewing insects (Li et al 2020). It was identified that, while JA is the central signal shaping the amplitude of convergent metabolic responses to both herbivories, ET fine-tunes the specificity of this metabolic response according to the herbivore diet breadth.…”

“…Hence, the important increases in M. sexta performance that were previously detected when feeding on ET signaling deficient plants likely translate from more profound and yet-to-explored deregulations of the host plant defense metabolism. In this respect, cross-talks between ET and other herbivory-induced hormonal sectors have been characterized at the molecular level (Wang, Li & Ecker 2002) and are likely to account for the deregulated defense response in N. attenuata lines rendered genetically insensitive to ET perception (von Dahl et al 2007;Li, Halitschke, Baldwin & Gaquerel 2020).…”

“…Nevertheless, besides the well-characterized function of ET in tuning the JA-induced nicotine production, its regulatory role over other classes of defense metabolites has remained poorly examined. In the case of phenolamides, a recent large-scale metabolomics study, which tested predictions of seminal hypotheses on the remodeling of specialized metabolite production during insect herbivory, has detected that ET signaling finely tunes the metabolic response of different Nicotiana species according to the herbivore species (Li et al 2020).…”

Genome-Wide Analysis Reveals Transcription Factors Regulated by Spider-Mite Feeding in Cucumber (Cucumis sativus)

“…This transcriptional regulation usually depends on the transcription and translation of TFs [ 16 ], although other factors such as chromatin-remodeling could also be involved [ 17 ]. The transcriptional changes in, for example, metabolism-associated genes finally result in an altered metabolic profile of the attacked plant [ 16 , 18 ].…”