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      Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores

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          Abstract

          Acylsugars are secondary metabolites exuded from type IV glandular trichomes that provide broad-spectrum insect suppression for Solanum pennellii Correll, a wild relative of cultivated tomato. Acylsugars produced by different S. pennellii accessions vary by sugar moieties (glucose or sucrose) and fatty acid side chains (lengths and branching patterns). Our objective was to determine which acylsugar compositions more effectively suppressed oviposition of the whitefly Bemisia tabaci (Gennadius) (Middle East—Asia Minor 1 Group), tobacco thrips, Frankliniella fusca (Hinds), and western flower thrips, Frankliniella occidentalis (Pergande). We extracted and characterized acylsugars from four S. pennellii accessions with different compositions, as well as from an acylsugar-producing tomato breeding line. We also fractionated the acylsugars of one S. pennellii accession to examine the effects of its components. Effects of acylsugars on oviposition were evaluated by administering a range of doses to oviposition sites of adult whiteflies and thrips in non-choice and choice bioassays, respectively. The acylsugars from S. pennellii accessions and the tomato breeding line demonstrated differential functionality in their ability to alter the distribution of whitefly oviposition and suppress oviposition on acylsugar treated substrates. Tobacco thrips were sensitive to all compositions while western flower thrips and whiteflies were more sensitive to acylsugars from a subset of S. pennellii accessions. It follows that acylsugars could thus mediate plant-enemy interactions in such a way as to affect evolution of host specialization, resistance specificity, and potentially host differentiation or local adaptation. The acylsugars from S. pennellii LA1376 were separated by polarity into two fractions that differed sharply for their sugar moieties and fatty acid side chains. These fractions had different efficacies, with neither having activity approaching that of the original exudate. When these two fractions were recombined, the effect on both whiteflies and thrips exceeded the sum of the two fractions’ effects, and was similar to that of the original exudate. These results suggest that increasing diversity of components within a mixture may increase suppression through synergistic interactions. This study demonstrates the potential for composition-specific deployment of acylsugars for herbivore oviposition suppression, either through in planta production by tomato lines, or as biocides applied by a foliar spray.

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          Natural products and plant disease resistance.

          R Dixon (2001)
          Plants elaborate a vast array of natural products, many of which have evolved to confer selective advantage against microbial attack. Recent advances in molecular technology, aided by the enormous power of large-scale genomics initiatives, are leading to a more complete understanding of the enzymatic machinery that underlies the often complex pathways of plant natural product biosynthesis. Meanwhile, genetic and reverse genetic approaches are providing evidence for the importance of natural products in host defence. Metabolic engineering of natural product pathways is now a feasible strategy for enhancement of plant disease resistance.
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            Acute, sublethal, antifeedant, and synergistic effects of monoterpenoid essential oil compounds on the tobacco cutworm, Spodoptera litura (Lep., Noctuidae).

            Monoterpenoids (terpenes and biogenically related phenols) commonly found in plant essential oils were tested for acute toxicity via topical application to tobacco cutworms (Spodoptera litura Fab.). The most toxic among 10 such compounds was thymol (LD(50) = 25.4 microg/larva) from garden thyme, Thymus vulgaris. The compounds were then tested for sublethal effects, specifically inhibition of larval growth after topical application of low doses. Among 6 compounds tested, an LD(10) dose reduced growth by 20% on average 3 days after administration. Feeding deterrence was determined using a cabbage leaf disk choice test. The most deterrent compound was thymol, with a DC(50) of 85.6 microg/cm(2) leaf disk area. Because minor constituents in complex essential oils have been suggested to act as synergists, binary mixtures of the compounds were tested for synergy vis à vis acute toxicity and feeding deterrence. trans-Anethole acted synergistically with thymol, citronellal, and alpha-terpineol, in terms of both acute toxicity and feeding deterrence. On the basis of these findings, several complex mixtures were developed and tested as leads for effective control agents. Candidate mixtures demonstrated good synergistic effects. The observed LD(50) of mixture 3 was 40.6 microg/larvae compared to an expected value of 74.6 microg/larvae. The result of this research is a proprietary product suitable for commercial production.
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              Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors.

              Plants deploy chemical defenses in complex mixtures, which are thought to be adaptive, but experimental tests have used artificial diets rather than plants. Herbivore attack on Nicotiana attenuata rapidly increases the production and accumulation of trypsin proteinase inhibitors (TPI) and the toxic alkaloid nicotine. By transgenically silencing their respective biosynthetic genes, we were able to abolish TPI activity and reduce inducible nicotine by 85%. Nicotine production was not affected by silencing pi or vice versa, and transformation did not alter levels of other metabolites examined. Spodoptera exigua, a native generalist herbivore that can compensate for heterologous TPI expression, performed better on TPI- or nicotine-deficient plants compared with the wild-type. Because of a compensatory feeding response to TPI when nicotine is absent, larvae performed better on nicotine-deficient plants than they did on plants silenced in both defenses. The antifeedant toxin, nicotine, prevents this compensatory response. We conclude that N. attenuata counters an insect adaptation with a defensive synergism.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 April 2016
                2016
                : 11
                : 4
                : e0153345
                Affiliations
                [1 ]Section of Plant Breeding and Genetics, School of Integrative Plant Science, Cornell University, Ithaca, New York, United States of America
                [2 ]Department of Entomology, North Carolina State University, Raleigh, North Carolina, United States of America
                [3 ]Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, United States of America
                Zhejiang University, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BML MAM GGK DAD. Performed the experiments: BML DAD DMD RH. Analyzed the data: TMC BML DAD. Contributed reagents/materials/analysis tools: MAM GGK AK. Wrote the paper: BML DAD TMC AK GGK MAM.

                [¤]

                Current address: School of Agriculture, Tennessee Technological University, Cookeville, Tennessee, United States of America

                Article
                PONE-D-15-34613
                10.1371/journal.pone.0153345
                4827819
                27065236
                464f2471-b541-4ed2-a9d7-8d5845c6c0a3
                © 2016 Leckie et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 August 2015
                : 28 March 2016
                Page count
                Figures: 3, Tables: 3, Pages: 19
                Funding
                This work was supported by the USDA National Institute of Food and Agriculture Special Research Grants Program - Pest Management Alternatives Research grant 2011-34381-30764 received by GK, MAM and AK and Coordinated Agricultural Project grant 2012-68004-20166 received by GK and MAM. Additional support provided by USDA National Institute of Food and Agriculture hatch funds 0223495 and 1000793 were received by MAM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Biology and Life Sciences
                Biochemistry
                Lipids
                Fatty Acids
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Fruits
                Tomatoes
                Biology and Life Sciences
                Organisms
                Plants
                Fruits
                Tomatoes
                Biology and Life Sciences
                Agriculture
                Pest Control
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Engineering and Technology
                Manufacturing Processes
                Surface Treatments
                Biology and Life Sciences
                Agriculture
                Pests
                Insect Pests
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Secondary Metabolites
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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                Uncategorized

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