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    Detection and imaging of the plant pathogen response by near-infrared fluorescent polyphenol sensors
    (Wiley, 2021-10-06)
    Plants use secondary metabolites such as polyphenols for chemical defense against pathogens and herbivores. Despite their importance in plant pathogen interactions and tolerance to diseases, it remains challenging to detect polyphenols in complex plant tissues. Here, we create molecular sensors for plant polyphenol imaging that are based on near‐infrared (NIR) fluorescent single‐wall carbon nanotubes (SWCNTs). We identified polyethylene glycol–phospholipids that render (6,5)‐SWCNTs sensitive (Kd=90 nM) to plant polyphenols (tannins, flavonoids, …), which red‐shift (up to 20 nm) and quench their emission (ca. 1000 nm). These sensors report changes in total polyphenol level after herbivore or pathogen challenge in crop plant systems (Soybean Glycine max) and leaf tissue extracts (Tococa spp.). We furthermore demonstrate remote chemical imaging of pathogen‐induced polyphenol release from roots of soybean seedlings over the time course of 24 h. This approach allows in situ visualization and understanding of the chemical plant defense in real time and paves the way for plant phenotyping for optimized polyphenol secretion.
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    Combined –omics framework reveals how ant symbionts benefit the Neotropical ant-plant Tococa quadrialata at different levels
    (Elsevier Inc., 2022-10-21)
    Ant-plant defensive mutualism is a widely studied phenomenon, where ants protect their host plants (myrmecophytes) against herbivores in return for the provision of nesting sites and food. However, few studies addressed the influence of ant colonization and herbivory on the plant's metabolism. We chose the Amazonian plant Tococa quadrialata , living in association with Azteca cf. tonduzi ants for an ant-exclusion study to reveal the chemistry behind this symbiosis. We found that colonized plants did not only benefit from protection but also from increased amino acid and nitrogen content, enabling better performance even in an herbivore-free environment. In contrast, ant-deprived T. quadrialata plants accumulated more ellagitannins, a major class of constitutive defense compounds. Moreover, herbivory-induced jasmonate-mediated defense responses, including the upregulation of signaling and defense genes and the emission of volatiles irrespective of colonization status. Altogether, we show how ant-colonization can influence the general and defense-related metabolism and performance of myrmecophytes.
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    Climate Change-Related Warming-Induced Shifts in Leaf Chemical Traits Favor Nutrition of the Specialist Herbivore Battus polydamas archidamas
    (Frontiers Media S.A., 2023-01-01)
    One of the major impacts of climate change is increasing global temperatures. Because warming is expected to affect plant morphological and chemical traits, it may therefore also influence plant interactions with other trophic levels, including herbivores. Here, we simulated a climate warming scenario of +2.7°C in the field using open-top chambers and assessed the effects of warming on plant performance (growth, leaf area, and chlorophyll), leaf nutrients (nitrogen and carbon), and primary (amino acids and carbohydrates) and secondary (toxic aristolochic acids) metabolites in the plant Aristolochia chilensis. We performed untargeted metabolomics analyses for estimating general changes in foliar metabolites between ambient control and warming-treated plants. Bioassays were additionally conducted to evaluate how changes in host plant chemistry affected growth and nutritional parameters in first-instar larvae of the specialist lepidopteran herbivore Battus polydamas archidamas. We found that warming did not significantly affect plant performance, but did result in significant changes in leaf nutrients, and primary and secondary metabolites, although in opposite directions. While primary metabolites (specifically, nitrogen-containing compounds) decreased in response to treatment, aristolochic acids increased. Untargeted metabolomics analyses showed that, of a total of 824 features, 50 were significantly different between ambient control and warming-treated plants; some of these were identified by MS/MS spectra as amino acids. Larvae feeding on warming-treated plants, showed significantly enhanced growth, food conversion efficiency, and lipid concentration. Our study contributes to current understanding of climate change impacts on trophic interactions, showing that projected temperature increases lead to changes in the resistance phenotype of the host plant, favoring nutrition and growth of a unique specialist herbivore.
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    Biosynthesis, Herbivore Induction, and Defensive Role of Phenylacetaldoxime Glucoside
    (Oxford University Press, 2023-08-16)
    Aldoximes are well-known metabolic precursors for plant defense compounds such as cyanogenic glycosides, glucosinolates, and volatile nitriles. They are also defenses themselves produced in response to herbivory; however, it is unclear whether aldoximes can be stored over a longer term as defense compounds and how plants protect themselves against the potential autotoxic effects of aldoximes. Here, we show that the Neotropical myrmecophyte tococa (Tococa quadrialata, recently renamed Miconia microphysca) accumulates phenylacetaldoxime glucoside (PAOx-Glc) in response to leaf herbivory. Sequence comparison, transcriptomic analysis, and heterologous expression revealed that 2 cytochrome P450 enzymes, CYP79A206 and CYP79A207, and the UDP-glucosyltransferase UGT85A123 are involved in the formation of PAOx-Glc in tococa. Another P450, CYP71E76, was shown to convert PAOx to the volatile defense compound benzyl cyanide. The formation of PAOx-Glc and PAOx in leaves is a very local response to herbivory but does not appear to be regulated by jasmonic acid signaling. In contrast to PAOx, which was only detectable during herbivory, PAOx-Glc levels remained high for at least 3 d after insect feeding. This, together with the fact that gut protein extracts of 3 insect herbivore species exhibited hydrolytic activity toward PAOx-Glc, suggests that the glucoside is a stable storage form of a defense compound that may provide rapid protection against future herbivory. Moreover, the finding that herbivory or pathogen elicitor treatment also led to the accumulation of PAOx-Glc in 3 other phylogenetically distant plant species suggests that the formation and storage of aldoxime glucosides may represent a widespread plant defense response.