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      A global invasion by the thrip, Frankliniella occidentalis: Current virus vector status and its management

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          Abstract

          Western flower thrip, Frankliniella occidentalis (Pergande), is among the most economically important agricultural pests globally, attacking a wide range of vegetable and horticultural crops. In addition to causing extensive crop damage, the species is notorious for vectoring destructive plant viruses, mainly belonging to the genera Orthotospovirus, Ilarvirus, Alphacarmovirus and Machlomovirus. Once infected by orthotospoviruses, thrips can remain virulent throughout their lifespan and continue transmitting viruses to host plants when and wherever they feed. These irruptive viral outbreaks in crops will permanently disrupt functional integrated pest management systems, and typically require a remedial treatment involving insecticides, contributing to further development of insecticide resistance. To mitigate against this continuing cycle, the most effective management is early and comprehensive surveillance of the pest species and recognition of plant viruses in the field. This review provides information on the pest status of F. occidentalis, discusses the current global status of the viruses vectored by this thrip species, examines the mechanisms involved in transmitting virus‐induced diseases by thrips, and reviews different management strategies, highlighting the potential management tactics developed for various cropping systems. The early surveillance and the utilization of potential methods for control of both F. occidentalis and viruses are proposed.

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          The use of push-pull strategies in integrated pest management.

          Push-pull strategies involve the behavioral manipulation of insect pests and their natural enemies via the integration of stimuli that act to make the protected resource unattractive or unsuitable to the pests (push) while luring them toward an attractive source (pull) from where the pests are subsequently removed. The push and pull components are generally nontoxic. Therefore, the strategies are usually integrated with methods for population reduction, preferably biological control. Push-pull strategies maximize efficacy of behavior-manipulating stimuli through the additive and synergistic effects of integrating their use. By orchestrating a predictable distribution of pests, efficiency of population-reducing components can also be increased. The strategy is a useful tool for integrated pest management programs reducing pesticide input. We describe the principles of the strategy, list the potential components, and present case studies reviewing work on the development and use of push-pull strategies in each of the major areas of pest control.
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            Insect vector-mediated transmission of plant viruses.

            The majority of plant-infecting viruses are transmitted to their host plants by vectors. The interactions between viruses and vector vary in duration and specificity but some common themes in vector transmission have emerged: 1) plant viruses encode structural proteins on the surface of the virion that are essential for transmission, and in some cases additional non-structural helper proteins that act to bridge the virion to the vector binding site; 2) viruses bind to specific sites in or on vectors and are retained there until they are transmitted to their plant hosts; and 3) viral determinants of vector transmission are promising candidates for translational research aimed at disrupting transmission or decreasing vector populations. In this review, we focus on well-characterized insect vector-transmitted viruses in the following genera: Caulimovirus, Crinivirus, Luteovirus, Geminiviridae, Reovirus, Tospovirus, and Tenuivirus. New discoveries regarding these genera have increased our understanding of the basic mechanisms of virus transmission by arthropods, which in turn have enabled the development of innovative strategies for breaking the transmission cycle. Copyright © 2015 Elsevier Inc. All rights reserved.
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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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                Author and article information

                Contributors
                sywu@ippcaas.cn
                Journal
                Insect Sci
                Insect Sci
                10.1111/(ISSN)1744-7917
                INS
                Insect Science
                John Wiley and Sons Inc. (Hoboken )
                1672-9609
                1744-7917
                23 October 2019
                August 2020
                : 27
                : 4 ( doiID: 10.1111/ins.v27.4 )
                : 626-645
                Affiliations
                [ 1 ] State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection Chinese Academy of Agricultural Sciences Beijing China
                [ 2 ] School of Horticulture and Plant Protection Yangzhou University Yangzhou Jiangsu Province China
                [ 3 ] Malheur Experiment Station Oregon State University Ontario OR USA
                Author notes
                [*] [* ]Correspondence: Sheng‐Yong Wu, State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China. Email: sywu@ 123456ippcaas.cn
                Author information
                https://orcid.org/0000-0003-2460-1583
                https://orcid.org/0000-0002-6771-9832
                Article
                INS12721
                10.1111/1744-7917.12721
                7318653
                31453663
                53183bc3-af49-49ef-abd9-3513e4d6523a
                © 2019 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 07 April 2019
                : 30 July 2019
                : 10 August 2019
                Page count
                Figures: 3, Tables: 0, Pages: 20, Words: 13592
                Funding
                Funded by: Chinese medicine resources
                Award ID: 2060302
                Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;
                Award ID: 31601604
                Funded by: National key research & developments (R&D) plan
                Award ID: 2016YFD0201002
                Categories
                Review
                Review
                Custom metadata
                2.0
                August 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.4 mode:remove_FC converted:26.06.2020

                global distribution,integrated pest management,invasion,thrips,viruses transmission

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