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      Rapid and Selective Absorption of Plant Defense Compounds From the Gut of a Sequestering Insect

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          Abstract

          Many herbivorous insects exploit defense compounds produced by their host plants for protection against predators. Ingested plant defense compounds are absorbed via the gut epithelium and stored in the body, a physiological process that is currently not well understood. Here, we investigated the absorption of plant defense compounds from the gut in the horseradish flea beetle, Phyllotreta armoraciae, a specialist herbivore known to selectively sequester glucosinolates from its brassicaceous host plants. Feeding experiments using a mixture of glucosinolates and other glucosides not found in the host plants showed a rapid and selective uptake of glucosinolates in adult beetles. In addition, we provide evidence that this uptake mainly takes place in the foregut, whereas the endodermal midgut is the normal region of absorption. Absorption via the foregut epithelium is surprising as the apical membrane is covered by a chitinous intima. However, we could show that this cuticular layer differs in its structure and overall thickness between P. armoraciae and a non-sequestering leaf beetle. In P. armoraciae, we observed a thinner cuticle with a less dense chitinous matrix, which might facilitate glucosinolate absorption. Our results show that a selective and rapid uptake of glucosinolates from the anterior region of the gut contributes to the selective sequestration of glucosinolates in P. armoraciae.

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          Most cited references47

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          R: a Lenguage and Environment for Statistical Computing

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            HemI: A Toolkit for Illustrating Heatmaps

            Recent high-throughput techniques have generated a flood of biological data in all aspects. The transformation and visualization of multi-dimensional and numerical gene or protein expression data in a single heatmap can provide a concise but comprehensive presentation of molecular dynamics under different conditions. In this work, we developed an easy-to-use tool named HemI (Heat map Illustrator), which can visualize either gene or protein expression data in heatmaps. Additionally, the heatmaps can be recolored, rescaled or rotated in a customized manner. In addition, HemI provides multiple clustering strategies for analyzing the data. Publication-quality figures can be exported directly. We propose that HemI can be a useful toolkit for conveniently visualizing and manipulating heatmaps. The stand-alone packages of HemI were implemented in Java and can be accessed at http://hemi.biocuckoo.org/down.php.
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              Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions.

              Cardenolides are remarkable steroidal toxins that have become model systems, critical in the development of theories for chemical ecology and coevolution. Because cardenolides inhibit the ubiquitous and essential animal enzyme Na⁺/K⁺-ATPase, most insects that feed on cardenolide-containing plants are highly specialized. With a huge diversity of chemical forms, these secondary metabolites are sporadically distributed across 12 botanical families, but dominate the Apocynaceae where they are found in > 30 genera. Studies over the past decade have demonstrated patterns in the distribution of cardenolides among plant organs, including all tissue types, and across broad geographic gradients within and across species. Cardenolide production has a genetic basis and is subject to natural selection by herbivores. In addition, there is strong evidence for phenotypic plasticity, with the biotic and abiotic environment predictably impacting cardenolide production. Mounting evidence indicates a high degree of specificity in herbivore-induced cardenolides in Asclepias. While herbivores of cardenolide-containing plants often sequester the toxins, are aposematic, and possess several physiological adaptations (including target site insensitivity), there is strong evidence that these specialists are nonetheless negatively impacted by cardenolides. While reviewing both the mechanisms and evolutionary ecology of cardenolide-mediated interactions, we advance novel hypotheses and suggest directions for future work. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                03 March 2022
                2022
                : 13
                : 846732
                Affiliations
                [1] 1Research Group Sequestration and Detoxification in Insects, Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology , Jena, Germany
                [2] 2Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology , Jena, Germany
                [3] 3Elektronenmikroskopisches Zentrum, Universitätsklinikum Jena , Jena, Germany
                [4] 4Institut für Zoologie und Evolutionsforschung, Friedrich-Schiller-Universität Jena , Jena, Germany
                [5] 5Department of Biochemistry, Max Planck Institute for Chemical Ecology , Jena, Germany
                Author notes

                Edited by: Chaoyang Zhao, University of California, United States

                Reviewed by: Wen Xie, Insititute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences (CAS), China; Qi Su, Yangtze University, China

                *Correspondence: Franziska Beran, fberan@ 123456ice.mpg.de

                Present address: Zhi-Ling Yang, Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China

                These authors have contributed equally to this work

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2022.846732
                8928188
                1995d8a1-1fc8-4157-8dd4-af6084f14091
                Copyright © 2022 Yang, Seitz, Grabe, Nietzsche, Richter, Reichelt, Beutel and Beran.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 December 2021
                : 31 January 2022
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 48, Pages: 11, Words: 7634
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                adaptation,cuticle,foregut,glucosinolate,plant defense,sequestration
                Anatomy & Physiology
                adaptation, cuticle, foregut, glucosinolate, plant defense, sequestration

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