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      The immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) when parasitized by Eretmocerus eremicus (Hymenoptera: Aphelinidae)

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          Abstract

          In insects, the innate immune system is subdivided into cellular and humoral defenses. When parasitoids attack insects, both reactions can be activated and notably, the phenoloxidase (PO) cascade and lytic activity are part of both cellular and humoral defenses. However, to our knowledge, no study has characterized any immune response of the whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) to the attack of Eretmocerus eremicus (Hymenoptera: Aphelinidae). Therefore, the first objective of the present study was to determine whether whitefly nymphs recently parasitized by E. eremicus exhibit any immune response. For this, we estimate the level of prophenoloxidase (proPO), phenoloxidase (PO), and lytic activity by colorimetric assays. A second objective was to assess whether the observed whitefly immune response could be related to a previously reported preference of the predator Geocoris punctipes (Hemiptera: Lygaeidae) for non-parasitized nymphs. We therefore offered non-parasitized and recently parasitized nymphs to the predator. Our results show that parasitism of whitefly nymphs by E. eremicus induced a highly estimated level of proPO and PO, and a lower level of lytic activity. In addition, we found that G. punctipes did not show a preference for non-parasitized over recently parasitized nymphs. The nymphs of T. vaporariorum activated the PO pathway against E. eremicus; however, the increase in proPO and PO levels was traded-off with decreased lytic activity. In addition, the previously reported preference for non-parasitized nymphs was not seen in our experiments, indicating that the induced immune response did not affect predator behavior by G. punctipes.

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          Biostatistical Analysis

          Designed for one/two-semester, junior/graduate-level courses in Biostatistics, Biometry, Quantitative Biology, or Statistics, the latest edition of this best-selling biostatistics text is both comprehensive and easy to read. It provides a broad and practical overview of the statistical analysis methods used by researchers to collect, summarize, analyze, and draw conclusions from biological research data. The Fourth Edition can serve as either an introduction to the discipline for beginning students or a comprehensive procedural reference for today's practitioners.
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            The host defense of Drosophila melanogaster.

            To combat infection, the fruit fly Drosophila melanogaster relies on multiple innate defense reactions, many of which are shared with higher organisms. These reactions include the use of physical barriers together with local and systemic immune responses. First, epithelia, such as those beneath the cuticle, in the alimentary tract, and in tracheae, act both as a physical barrier and local defense against pathogens by producing antimicrobial peptides and reactive oxygen species. Second, specialized hemocytes participate in phagocytosis and encapsulation of foreign intruders in the hemolymph. Finally, the fat body, a functional equivalent of the mammalian liver, produces humoral response molecules including antimicrobial peptides. Here we review our current knowledge of the molecular mechanisms underlying Drosophila defense reactions together with strategies evolved by pathogens to evade them.
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              The prophenoloxidase-activating system in invertebrates.

              A major innate defense system in invertebrates is the melanization of pathogens and damaged tissues. This important process is controlled by the enzyme phenoloxidase (PO) that in turn is regulated in a highly elaborate manner for avoiding unnecessary production of highly toxic and reactive compounds. Recent progress, especially in arthropods, in the elucidation of mechanisms controlling the activation of zymogenic proPO into active PO by a cascade of serine proteinases and other factors is reviewed. The proPO-activating system (proPO system) is triggered by the presence of minute amounts of compounds of microbial origins, such as beta-1,3-glucans, lipopolysaccharides, and peptidoglycans, which ensures that the system will become active in the presence of potential pathogens. The presence of specific proteinase inhibitors prevents superfluous activation. Concomitant with proPO activation, many other immune reactions will be produced, such as the generation of factors with anti-microbial, cytotoxic, opsonic, or encapsulation-promoting activities.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 December 2023
                2023
                : 18
                : 12
                : e0296157
                Affiliations
                [1 ] Laboratorio de Ecología Evolutiva, ENES, Unidad Morelia, UNAM, Morelia, Michoacán, México
                [2 ] Laboratorio de Control Biológico (Lab CB-AIFEN), Departamento de Producción Agrícola, CUCBA, Universidad de Guadalajara, Zapopan, Jalisco, México
                Uppsala University, SWEDEN
                Author notes

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

                ‡ JCG and RRR are joint senior authors on this work.

                Author information
                https://orcid.org/0000-0003-1310-0484
                Article
                PONE-D-23-16522
                10.1371/journal.pone.0296157
                10734938
                38128052
                7253b9eb-c437-471c-bdfd-7fab8111c444
                © 2023 Contreras-Garduño 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
                : 29 May 2023
                : 6 December 2023
                Page count
                Figures: 3, Tables: 1, Pages: 15
                Funding
                Funded by: CONACyT sabbatical scholarship
                Award ID: 740591
                Award Recipient :
                Funded by: PRO-SNI and Fortalecimiento programs (UdG)
                Award ID: (2019-2022)
                Award Recipient :
                Funded by: Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica
                Award ID: PAPIIT, IA205318
                Award Recipient :
                CONACyT sabbatical scholarship N° 740591 to RRR. PRO-SNI and Fortalecimiento programs (UdG2019-2022) to RRR. Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT, IA205318) to JCG. 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
                Developmental Biology
                Life Cycles
                Nymphs
                Biology and Life Sciences
                Immunology
                Immune Response
                Medicine and Health Sciences
                Immunology
                Immune Response
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Biology and Life Sciences
                Zoology
                Entomology
                Insects
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Levodopa
                Biology and Life Sciences
                Biochemistry
                Neurochemistry
                Neurochemicals
                Levodopa
                Biology and Life Sciences
                Neuroscience
                Neurochemistry
                Neurochemicals
                Levodopa
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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