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      Combined influence of Bt rice and rice dwarf virus on biological parameters of a non-target herbivore, Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae)

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          Abstract

          The advent of genetically modified (GM) Bt rice creates the possibility of interactions among Bt crops, crop pathogens and non-target herbivores. In particular, information on how pathogen-infected Bt-expressing plants will influence non-target herbivores is necessary to predict the sustainability of GM cropping systems. Laboratory bioassays were conducted to evaluate the potential combined impacts of rice dwarf virus (RDV) and two Bt rice lines, T1C-19 (Cry1C) and T2A-1 (Cry2A), on non-target green rice leafhopper (GRLH), Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae). In the first experiment, GRLHs feeding preference tests on Bt rice lines compared to a parental control rice line, MH63, were conducted. As rice plants were uninfected with RDV, GRLHs generally preferred the control MH63 line over the two Bt lines during the initial 8 h, with no significant preference during the following 64 h. As rice plants were infected with RDV, there were no clear preferences between the Bt rice lines and the control MH63 line. In the second experiment, we assessed the combined influence of RDV-infection status and Bt rice lines on GRLH biological parameters. Egg duration, adult weights, and male adult longevity were significantly affected on RDV-infected Bt rice. Other parameters, egg hatching rate, nymph survival and fecundity were not significantly influenced. We infer that interaction effect among two testing Bt rice lines and RDV will not lead to enlarged pest populations, thus demonstrating that growing these two Bt rice lines will poses negligible risk to GRLH in sustainable rice agroecosystems. Long-term field experiments to monitor the population dynamics of GRLHs at large scale need to be carried out to confirm the current results.

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          Insect vector interactions with persistently transmitted viruses.

          The majority of described plant viruses are transmitted by insects of the Hemipteroid assemblage that includes aphids, whiteflies, leafhoppers, planthoppers, and thrips. In this review we highlight progress made in research on vector interactions of the more than 200 plant viruses that are transmitted by hemipteroid insects beginning a few hours or days after acquisition and for up to the life of the insect, i.e., in a persistent-circulative or persistent-propagative mode. These plant viruses move through the insect vector, from the gut lumen into the hemolymph or other tissues and finally into the salivary glands, from which these viruses are introduced back into the plant host during insect feeding. The movement and/or replication of the viruses in the insect vectors require specific interactions between virus and vector components. Recent investigations have resulted in a better understanding of the replication sites and tissue tropism of several plant viruses that propagate in insect vectors. Furthermore, virus and insect proteins involved in overcoming transmission barriers in the vector have been identified for some virus-vector combinations.
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            Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services.

            Over the past 16 years, vast plantings of transgenic crops producing insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have helped to control several major insect pests and reduce the need for insecticide sprays. Because broad-spectrum insecticides kill arthropod natural enemies that provide biological control of pests, the decrease in use of insecticide sprays associated with Bt crops could enhance biocontrol services. However, this hypothesis has not been tested in terms of long-term landscape-level impacts. On the basis of data from 1990 to 2010 at 36 sites in six provinces of northern China, we show here a marked increase in abundance of three types of generalist arthropod predators (ladybirds, lacewings and spiders) and a decreased abundance of aphid pests associated with widespread adoption of Bt cotton and reduced insecticide sprays in this crop. We also found evidence that the predators might provide additional biocontrol services spilling over from Bt cotton fields onto neighbouring crops (maize, peanut and soybean). Our work extends results from general studies evaluating ecological effects of Bt crops by demonstrating that such crops can promote biocontrol services in agricultural landscapes.
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              Plants, viruses and the environment: Ecology and mutualism.

              Since the discovery of Tobacco mosaic virus nearly 120 years ago, most studies on viruses have focused on their roles as pathogens. Virus ecology takes a different look at viruses, from the standpoint of how they affect their hosts׳ interactions with the environment. Using the framework of symbiotic relationships helps put the true nature of viruses into perspective. Plants clearly have a long history of relationships with viruses that have shaped their evolution. In wild plants viruses are common but usually asymptomatic. In experimental studies plant viruses are sometimes mutualists rather than pathogens. Virus ecology is closely tied to the ecology of their vectors, and the behavior of insects, critical for transmission of many plant viruses, is impacted by virus-plant interactions. Virulence is probable not beneficial for most host-virus interactions, hence commensal and mutualistic relationships are almost certainly common, in spite of the paucity of literature on beneficial viruses.
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                Author and article information

                Contributors
                Role: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Resources
                Role: Software
                Role: Software
                Role: Software
                Role: Software
                Role: Supervision
                Role: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: Supervision
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 July 2017
                2017
                : 12
                : 7
                : e0181258
                Affiliations
                [1 ] State Key Laboratory of Rice Biology, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, China
                [2 ] State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
                [3 ] USDA/Agricultural Research Service, Biological Control of Insects Research Laboratory, Columbia MO, United States of America
                Institut Sophia Agrobiotech, FRANCE
                Author notes

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

                Author information
                http://orcid.org/0000-0003-4937-8867
                Article
                PONE-D-16-43097
                10.1371/journal.pone.0181258
                5533439
                28753622
                43657a5d-67dc-42df-b1d7-6c5a4f79215f
                © 2017 Wang 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 October 2016
                : 28 June 2017
                Page count
                Figures: 1, Tables: 2, Pages: 11
                Funding
                Funded by: Special Research Projects for Developing Transgenic Plants, China
                Award ID: 2014ZX08011-001
                Award Recipient :
                Funded by: Special Research Projects for Developing Transgenic Plants, China
                Award ID: 2016ZX08011-001
                Award Recipient :
                Funded by: National Program on Key Basic Research Projects
                Award ID: 2014CB138404
                Award Recipient :
                Financial supports were provided by the Special Research Projects for Developing Transgenic Plants, China (2016ZX08011-001, and 2014ZX08011-001) and the National Program on Key Basic Research Projects (973 Program, 2014CB138404), as well as the Rice Pests Management Research Group of the Agricultural Science and Technology Innovation Program, China. 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
                Organisms
                Plants
                Grasses
                Rice
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Rice
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Nymphs
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Fecundity
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Plant-Herbivore Interactions
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Pathogens
                Plant Viral Pathogens
                Biology and Life Sciences
                Organisms
                Plants
                Seedlings
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