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      ABC transporter functions as a pacemaker for sequestration of plant glucosides in leaf beetles

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          Abstract

          Plant-herbivore interactions dominate the planet’s terrestrial ecology. When it comes to host–plant specialization, insects are among the most versatile evolutionary innovators, able to disarm multiple chemical plant defenses. Sequestration is a widespread strategy to detoxify noxious metabolites, frequently for the insect’s own benefit against predation. In this study, we describe the broad-spectrum ATP-binding cassette transporter CpMRP of the poplar leaf beetle, Chrysomela populi as the first candidate involved in the sequestration of phytochemicals in insects. CpMRP acts in the defensive glands of the larvae as a pacemaker for the irreversible shuttling of pre-selected metabolites from the hemolymph into defensive secretions. Silencing CpMRP in vivo creates a defenseless phenotype, indicating its role in the secretion process is crucial. In the defensive glands of related leaf beetle species, we identified sequences similar to CpMRP and assume therefore that exocrine gland-based defensive strategies, evolved by these insects to repel their enemies, rely on ABC transporters as a key element.

          DOI: http://dx.doi.org/10.7554/eLife.01096.001

          eLife digest

          For millions of years, plant feeding insects have been locked in an arms race with the plants they consume. Plants have evolved defensive strategies such as the ability to produce noxious chemicals that deter insects, while many insects have evolved the means to thwart this defense and even turn it to their own advantage. The larvae of the poplar leaf beetle, Chrysomela populi, sequester toxic plant compounds in specialized glands on their backs and use these compounds to defend themselves against predators. The glands are lined with chemically inert chitin, the substance that makes up the insect exoskeleton, and the deterrent chemicals are released whenever the insect is threatened.

          Now, Strauss et al. have identified a key transport protein used by the larvae to move toxic plant compounds to these glands. This transport protein belongs to a family of membrane proteins called ABC transporters, which help to shuttle substances out of cells or into cell organelles using energy produced by the hydrolysis of ATP molecules. The gene for this transporter is expressed in the glands of the leaf beetles at levels 7,000 times higher than elsewhere in the larvae.

          Larvae that lack a functional version of the transporter gene continue to grow, but are unable to defend themselves against predators. Similar genes are found in other species of leaf beetle, suggesting that this type of transporter has been retained throughout evolution. Moreover, the transporter is not specific to a particular plant toxin; this enables leaf beetles to eat many different types of plants and boosts their chances of survival should a previous food source disappear.

          DOI: http://dx.doi.org/10.7554/eLife.01096.002

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          Most cited references39

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          Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics.

          Xenobiotic resistance in insects has evolved predominantly by increasing the metabolic capability of detoxificative systems and/or reducing xenobiotic target site sensitivity. In contrast to the limited range of nucleotide changes that lead to target site insensitivity, many molecular mechanisms lead to enhancements in xenobiotic metabolism. The genomic changes that lead to amplification, overexpression, and coding sequence variation in the three major groups of genes encoding metabolic enzymes, i.e., cytochrome P450 monooxygenases (P450s), esterases, and glutathione-S-transferases (GSTs), are the focus of this review. A substantial number of the adaptive genomic changes associated with insecticide resistance that have been characterized to date are transposon mediated. Several lines of evidence suggest that P450 genes involved in insecticide resistance, and perhaps insecticide detoxification genes in general, may share an evolutionary association with genes involved in allelochemical metabolism. Differences in the selective regime imposed by allelochemicals and insecticides may account for the relative importance of regulatory or structural mutations in conferring resistance.
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            Butterflies and Plants: A Study in Coevolution

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              The genome of the model beetle and pest Tribolium castaneum.

              Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                03 December 2013
                2013
                : 2
                : e01096
                Affiliations
                [1 ]Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology , Jena, Germany
                [2 ]Department of Ophthalmology, University Hospital Jena , Jena, Germany
                Wageningen University , The Netherlands
                Wageningen University , The Netherlands
                Author notes
                [* ]For correspondence: astrauss@ 123456ice.mpg.de (ASS);
                [* ]For correspondence: aburse@ 123456ice.mpg.de (AB)
                Article
                01096
                10.7554/eLife.01096
                3843118
                24302568
                3d844008-c8f8-4c8f-8cdc-2e3095dd765b
                Copyright © 2013, Strauss et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 17 June 2013
                : 24 October 2013
                Funding
                Funded by: Max Planck Society
                Award Recipient :
                Funded by: Deutsche Forschungsgesellschaft
                Award ID: BU1862/2-1
                Award Recipient :
                Funded by: University Hospital Jena
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Biochemistry
                Ecology
                Custom metadata
                0.7
                A transport protein enables leaf beetle larvae to take up and store plant toxins and use them as part of their own defense strategy.

                Life sciences
                chrysomela populi,phaedon cochleariae,chrysomela lapponica,chemical defense,rna interference,fluorescence microscopy,other

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