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Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores
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 fa...
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Published in: | PloS one 2016-04, Vol.11 (4), p.e0153345-e0153345 |
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description | 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, o |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0153345</identifier><identifier>PMID: 27065236</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acylation ; Acylsugars ; Analysis ; Animals ; Bemisia tabaci ; Bioassays ; Biocides ; Biological Assay ; Biology and Life Sciences ; Breeding ; Chain branching ; Chains ; Composition effects ; Datura wrightii ; Engineering and Technology ; Evolution ; Evolutionary biology ; Exudation ; Fatty acids ; Female ; Flowers & plants ; Fruit cultivation ; Genetics ; Hemiptera ; Hemiptera - physiology ; Herbivores ; Herbivory ; Insect Control ; Insects ; Medicine and Health Sciences ; Metabolites ; Oils & fats ; Oviposition ; Oviposition - physiology ; Pest control ; Petunia ; Plant breeding ; Plant metabolites ; Plant resistance ; Plant sciences ; Polarity ; Secondary metabolites ; Solanaceae ; Solanum ; Solanum lycopersicum ; Solanum lycopersicum - metabolism ; Solanum lycopersicum - parasitology ; Specialization ; Spodoptera litura ; Substrates ; Sucrose ; Sucrose - metabolism ; Sugar ; Thripidae ; Thysanoptera ; Thysanoptera - physiology ; Tobacco ; Tomato breeding ; Tomatoes ; Trichomes ; Viruses ; Western flower thrips</subject><ispartof>PloS one, 2016-04, Vol.11 (4), p.e0153345-e0153345</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Leckie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Leckie et al 2016 Leckie et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-884bfa091646566bd71da01b350595531d7b58f1cf398fef6199c5ed3b90cd143</citedby><cites>FETCH-LOGICAL-c692t-884bfa091646566bd71da01b350595531d7b58f1cf398fef6199c5ed3b90cd143</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1780143127/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1780143127?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27065236$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Wang, Xiao-Wei</contributor><creatorcontrib>Leckie, Brian M</creatorcontrib><creatorcontrib>D'Ambrosio, Damon A</creatorcontrib><creatorcontrib>Chappell, Thomas M</creatorcontrib><creatorcontrib>Halitschke, Rayko</creatorcontrib><creatorcontrib>De Jong, Darlene M</creatorcontrib><creatorcontrib>Kessler, André</creatorcontrib><creatorcontrib>Kennedy, George G</creatorcontrib><creatorcontrib>Mutschler, Martha A</creatorcontrib><title>Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>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.</description><subject>Acylation</subject><subject>Acylsugars</subject><subject>Analysis</subject><subject>Animals</subject><subject>Bemisia tabaci</subject><subject>Bioassays</subject><subject>Biocides</subject><subject>Biological Assay</subject><subject>Biology and Life Sciences</subject><subject>Breeding</subject><subject>Chain branching</subject><subject>Chains</subject><subject>Composition effects</subject><subject>Datura wrightii</subject><subject>Engineering and Technology</subject><subject>Evolution</subject><subject>Evolutionary biology</subject><subject>Exudation</subject><subject>Fatty acids</subject><subject>Female</subject><subject>Flowers & plants</subject><subject>Fruit cultivation</subject><subject>Genetics</subject><subject>Hemiptera</subject><subject>Hemiptera - physiology</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Insect Control</subject><subject>Insects</subject><subject>Medicine and Health Sciences</subject><subject>Metabolites</subject><subject>Oils & fats</subject><subject>Oviposition</subject><subject>Oviposition - physiology</subject><subject>Pest control</subject><subject>Petunia</subject><subject>Plant breeding</subject><subject>Plant metabolites</subject><subject>Plant resistance</subject><subject>Plant sciences</subject><subject>Polarity</subject><subject>Secondary metabolites</subject><subject>Solanaceae</subject><subject>Solanum</subject><subject>Solanum lycopersicum</subject><subject>Solanum lycopersicum - metabolism</subject><subject>Solanum lycopersicum - parasitology</subject><subject>Specialization</subject><subject>Spodoptera litura</subject><subject>Substrates</subject><subject>Sucrose</subject><subject>Sucrose - metabolism</subject><subject>Sugar</subject><subject>Thripidae</subject><subject>Thysanoptera</subject><subject>Thysanoptera - physiology</subject><subject>Tobacco</subject><subject>Tomato breeding</subject><subject>Tomatoes</subject><subject>Trichomes</subject><subject>Viruses</subject><subject>Western flower thrips</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9-L1DAQx4so3rn6H4gWBNGHXZPmR9MXYTk9b-FgwVVfQ5om3SzdpJe0i_vfm7q9Yyv3IHlIyHzmO5mZTJK8hmABUQ4_7VzvrWgWrbNqASBBCJMnySUsUDanGUBPz84XyYsQdgAQxCh9nlxkOaAkQ_Qy2X4xWiuvbGdEkwpbpZujVb42oTMyve6t7IyLYUx3TJ1Ol_LYhL4WPqTGppu-bb0Kwdg6XR9M64IZ6LQ8pisblOzSG-VLc3ARepk806IJ6tW4z5Kf119_XN3Mb9ffVlfL27mkRdbNGcOlFqCAFFNCaVnlsBIAlogAUhCCYJWXhGkoNSqYVprCopBEVagsgKwgRrPk7Um3bVzgY5EChzkD0QqzPBKrE1E5seOtN3vhj9wJw_9eOF9z4WP2jeIAkULmmCmiMqwpYBhVpVBCVZnIREmj1ucxWl_uVSVjHb1oJqJTizVbXrsDxyzLWezPLPkwCnh316vQ8b0JUjWNsMr1p3czGJ8xxHr3D_p4diNVi5iAsdrFuHIQ5UtMEMYMUxipxSNUXJXaGxl_lDbxfuLwceIQmU797mrRh8BXm-__z65_Tdn3Z-xWiabbBtf0wz8KUxCfQOldCF7phyJDwIeBuK8GHwaCjwMR3d6cN-jB6X4C0B-63QbY</recordid><startdate>20160411</startdate><enddate>20160411</enddate><creator>Leckie, Brian M</creator><creator>D'Ambrosio, Damon A</creator><creator>Chappell, Thomas M</creator><creator>Halitschke, Rayko</creator><creator>De Jong, Darlene M</creator><creator>Kessler, André</creator><creator>Kennedy, George G</creator><creator>Mutschler, Martha A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160411</creationdate><title>Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores</title><author>Leckie, Brian M ; D'Ambrosio, Damon A ; Chappell, Thomas M ; Halitschke, Rayko ; De Jong, Darlene M ; Kessler, André ; Kennedy, George G ; Mutschler, Martha A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-884bfa091646566bd71da01b350595531d7b58f1cf398fef6199c5ed3b90cd143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Acylation</topic><topic>Acylsugars</topic><topic>Analysis</topic><topic>Animals</topic><topic>Bemisia tabaci</topic><topic>Bioassays</topic><topic>Biocides</topic><topic>Biological Assay</topic><topic>Biology and Life Sciences</topic><topic>Breeding</topic><topic>Chain branching</topic><topic>Chains</topic><topic>Composition effects</topic><topic>Datura wrightii</topic><topic>Engineering and Technology</topic><topic>Evolution</topic><topic>Evolutionary biology</topic><topic>Exudation</topic><topic>Fatty acids</topic><topic>Female</topic><topic>Flowers & plants</topic><topic>Fruit cultivation</topic><topic>Genetics</topic><topic>Hemiptera</topic><topic>Hemiptera - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>ProQuest Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Leckie, Brian M</au><au>D'Ambrosio, Damon A</au><au>Chappell, Thomas M</au><au>Halitschke, Rayko</au><au>De Jong, Darlene M</au><au>Kessler, André</au><au>Kennedy, George G</au><au>Mutschler, Martha A</au><au>Wang, Xiao-Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-04-11</date><risdate>2016</risdate><volume>11</volume><issue>4</issue><spage>e0153345</spage><epage>e0153345</epage><pages>e0153345-e0153345</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27065236</pmid><doi>10.1371/journal.pone.0153345</doi><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2016-04, Vol.11 (4), p.e0153345-e0153345 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1780143127 |
source | PubMed Central Free; Publicly Available Content Database |
subjects | Acylation Acylsugars Analysis Animals Bemisia tabaci Bioassays Biocides Biological Assay Biology and Life Sciences Breeding Chain branching Chains Composition effects Datura wrightii Engineering and Technology Evolution Evolutionary biology Exudation Fatty acids Female Flowers & plants Fruit cultivation Genetics Hemiptera Hemiptera - physiology Herbivores Herbivory Insect Control Insects Medicine and Health Sciences Metabolites Oils & fats Oviposition Oviposition - physiology Pest control Petunia Plant breeding Plant metabolites Plant resistance Plant sciences Polarity Secondary metabolites Solanaceae Solanum Solanum lycopersicum Solanum lycopersicum - metabolism Solanum lycopersicum - parasitology Specialization Spodoptera litura Substrates Sucrose Sucrose - metabolism Sugar Thripidae Thysanoptera Thysanoptera - physiology Tobacco Tomato breeding Tomatoes Trichomes Viruses Western flower thrips |
title | Differential and Synergistic Functionality of Acylsugars in Suppressing Oviposition by Insect Herbivores |
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