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      Acylsugar amount and fatty acid profile differentially suppress oviposition by western flower thrips, Frankliniella occidentalis, on tomato and interspecific hybrid flowers

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          Abstract

          Tomatoes ( Solanum lycopersicum L.) have been bred to exude higher amounts or different types of the specialized plant metabolites, acylsugars, from type IV trichomes. Acylsugars are known to deter several herbivorous insect pests, including the western flower thrips (WFT), Frankliniella occidentalis (Pergande); however, all previous studies investigated the effect of acylsugars on leaves, or acylsugar extracts obtained from leaves. In spite of the WFT predilection for flowers, there is a gap in knowledge about flower defenses against thrips damage. This is especially important in light of their capacity to acquire and inoculate viruses in the genus Orthotospovirus, such as Tomato spotted wilt orthotospovirus (TSWV), in flowers. Therefore, we turned our attention to assessing thrips oviposition differences on flowers of 14 entries, including 8 interspecific hybrids, 5 tomato lines bred for specific acylsugar-related characteristics (type IV trichome densities, acylsugar amount, sugar moiety and fatty acid profile), and a fresh market tomato hybrid, Mt. Spring, which only produces trace amounts of acylsugars. Our results show that the density of the acylsugar droplet bearing type IV trichomes is greatest on sepals, relative to other flower structures, and accordingly, WFT avoids oviposition on sepals in favor of trichome-sparse petals. In concordance with past studies, acylsugar amount was the most important acylsugar-related characteristic suppressing WFT oviposition. Certain acylsugar fatty acids, specifically i-C5, i-C9 and i-C11, were also significantly associated with changes in WFT oviposition. These results support continued breeding efforts to increase acylsugar amounts and explore modifications of fatty acid profile and their roles in deterring thrips oviposition. The finding that acylsugar production occurs and reduces thrips oviposition in tomato flowers will be important in efforts to use acylsugar-mediated resistance to reduce incidence of orthotospoviruses such as TSWV in tomato by deterring virus transmission and development of thrips vector populations in the crop.

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          Infection with a plant virus modifies vector feeding behavior.

          Vector infection by some animal-infecting parasites results in altered feeding that enhances transmission. Modification of vector behavior is of broad adaptive significance, as parasite fitness relies on passage to a new host, and vector feeding is nearly always essential for transmission. Although several plant viruses infect their insect vectors, we have shown that vector infection by a plant virus alters feeding behavior. Here we show that infection with Tomato spotted wilt virus (TSWV), type member of the only plant-infecting genus in the Bunyaviridae, alters the feeding behavior of its thrips vector, Frankliniella occidentalis (Pergande). Male thrips infected with TSWV fed more than uninfected males, with the frequency of all feeding behaviors increasing by up to threefold, thus increasing the probability of virus inoculation. Importantly, infected males made almost three times more noningestion probes (probes in which they salivate, but leave cells largely undamaged) compared with uninfected males. A functional cell is requisite for TSWV infection and cell-to-cell movement; thus, this behavior is most likely to establish virus infection. Some animal-infecting members of the Bunyaviridae (La Crosse virus and Rift Valley fever virus) also cause increased biting rates in infected vectors. Concomitantly, these data support the hypothesis that capacity to modify vector feeding behavior is a conserved trait among plant- and animal-infecting members of the Bunyaviridae that evolved as a mechanism to enhance virus transmission. Our results underscore the evolutionary importance of vector behavioral modification to diverse parasites with host ranges spanning both plant and animal kingdoms.
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            Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon.

            Insect-plant interactions involving the cultivated tomato and its relatives in the genus Lycopersicon have been intensively studied for several decades, resulting in one of the best documented and in-depth examples of the mechanistic complexities of insect-plant interactions, which encompass both herbivores and their natural enemies. Trichome-mediated defenses are particularly significant in L. hirsutum f. glabratum and have been extensively implicated in negative tritrophic effects mediated by direct contact of parasitoids and predators with trichomes, as well as indirect effects mediated through their hosts or prey. Both constitutive and inducible defense traits of L. esculentum exert effects on selected parasitoids and predators. The effects of any particular plant defense trait on parasitoids and predators depend on the specific attributes of the plant trait and the details of the physical, biochemical, and behavioral interaction between the natural enemy, its host (prey), and the plant.
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              Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation.

              Plant glandular trichomes exude secondary metabolites with defensive functions, but these epidermal protuberances are surprisingly the first meal of Lepidopteran herbivores on Nicotiana attenuata. O-acyl sugars, the most abundant metabolite of glandular trichomes, impart a distinct volatile profile to the body and frass of larvae that feed on them. The headspace composition of Manduca sexta larvae is dominated by the branched chain aliphatic acids hydrolyzed from ingested O-acyl sugars, which waxes and wanes rapidly with trichome ingestion. In native habitats a ground-hunting predator, the omnivorous ant Pogonomyrmex rugosus, but not the big-eyed bug Geocoris spp., use these volatile aliphatic acids to locate their prey.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: Visualization
                Role: InvestigationRole: MethodologyRole: Visualization
                Role: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                31 July 2018
                2018
                : 13
                : 7
                : e0201583
                Affiliations
                [1 ] Department of Entomology and Nematology, University of California, Davis, California, United States of America
                [2 ] Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York, United States of America
                [3 ] Department of Plant Pathology and Microbiology, Agriculture and Life Sciences, Texas A&M University, College Station, Texas, United States of America
                [4 ] Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina, United States of America
                Chinese Academy of Agricultural Sciences Institute of Plant Protection, CHINA
                Author notes

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

                Author information
                http://orcid.org/0000-0002-2992-5934
                Article
                PONE-D-18-05245
                10.1371/journal.pone.0201583
                6067722
                30063755
                147031e0-53b7-4a45-9a0a-5e8c3580d9c1
                © 2018 Ben-Mahmoud 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
                : 16 February 2018
                : 18 July 2018
                Page count
                Figures: 5, Tables: 2, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100005825, National Institute of Food and Agriculture;
                Award ID: 2012-68004-20166
                Award Recipient :
                Funding for this research was provided by AFRI NIFA Coordinated Agricultural Project 2012-68004-20166. The funder 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
                Plant Science
                Plant Anatomy
                Flowers
                Biology and Life Sciences
                Biochemistry
                Lipids
                Fatty Acids
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Tomatoes
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Sepals
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Trichomes
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Petals
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Flowering Plants
                Custom metadata
                We have made all relevant data available within the paper and its Supporting Information files.

                Uncategorized
                Uncategorized

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