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      An adenylyl cyclase like-9 gene ( NlAC9) influences growth and fecundity in the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)

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          Abstract

          The cAMP/PKA intracellular signaling pathway is launched by adenylyl cyclase (AC) conversion of adenosine triphosphate (ATP) to 3', 5'-cyclic AMP (cAMP) and cAMP-dependent activation of PKA. Although this pathway is very well known in insect physiology, there is little to no information on it in some very small pest insects, such as the brown planthopper (BPH), Nilaparvata lugens Stål. BPH is a destructive pest responsible for tremendous crop losses in rice cropping systems. We are investigating the potentials of novel pest management technologies from RNA interference perspective. Based on analysis of transcriptomic data, the BPH AC like-9 gene ( NlAC9) was up-regulated in post-mating females, which led us to pose the hypothesis that NlAC9 is a target gene that would lead to reduced BPH fitness and populations. Targeting NlAC9 led to substantially decreased soluble ovarian protein content, yeast-like symbiont abundance, and vitellogenin gene expression, accompanied with stunted ovarian development and body size. Eggs laid were decreased and oviposition period shortened. Taken together, our findings indicated that NlAC9 exerted pronounced effects on female fecundity, growth and longevity, which strongly supports our hypothesis.

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          Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review.

          RNA interference already proved its usefulness in functional genomic research on insects, but it also has considerable potential for the control of pest insects. For this purpose, the insect should be able to autonomously take up the dsRNA, for example through feeding and digestion in its midgut. In this review we bring together current knowledge on the uptake mechanisms of dsRNA in insects and the potential of RNAi to affect pest insects. At least two pathways for dsRNA uptake in insects are described: the transmembrane channel-mediated uptake mechanism based on Caenorhabditis elegans' SID-1 protein and an 'alternative' endocytosis-mediated uptake mechanism. In the second part of the review dsRNA feeding experiments on insects are brought together for the first time, highlighting the achievement of implementing RNAi in insect control with the first successful experiments in transgenic plants and the diversity of successfully tested insect orders/species and target genes. We conclude with points of discussion and concerns regarding further research on dsRNA uptake mechanisms and the promising application possibilities for RNAi in insect control. Copyright (c) 2009 Elsevier Ltd. All rights reserved.
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            Learning and memory in honeybees: from behavior to neural substrates.

            Learning and memory in honeybees is analyzed on five levels, using a top-down approach. (a) Observatory learning is applied during navigation and dance communication. (b) Local cues at the feeding site are learned associatively. (c) Classical conditioning of the proboscis extension response to olfactory stimuli provides insight into behavioral, neural, and neuropharmacological mechanisms of associative learning. (d) At the neural level, the pathways coding the conditioned and the unconditioned stimulus are identified. The reinforcing function of the unconditioned stimulus is traced to a particular neuron. (e) At the cellular level, the cAMP pathway is found to be critically involved. Nitric oxide is an essential mediator for the transfer from short- to long-term memory.
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              A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis.

              Many pathogenic organisms and their toxins target host cell receptors, the consequence of which is altered signaling events that lead to aberrant activity or cell death. A significant body of literature describes various molecular and cellular aspects of toxins associated with bacterial invasion, colonization, and host cell disruption. However, there is little information on the molecular and cellular mechanisms associated with the insecticidal action of Bacillus thuringiensis (Bt) Cry toxins. Recently, we reported that the Cry1Ab toxin produced by Bt kills insect cells by activating a Mg(2+)-dependent cytotoxic event upon binding of the toxin to its receptor BT-R(1). Here we show that binding of Cry toxin to BT-R(1) provokes cell death by activating a previously undescribed signaling pathway involving stimulation of G protein (G(alphas)) and adenylyl cyclase, increased cAMP levels, and activation of protein kinase A. Induction of the adenylyl cyclase/protein kinase A pathway is manifested by sequential cytological changes that include membrane blebbing, appearance of ghost nuclei, cell swelling, and lysis. The discovery of a toxin-induced cell death pathway specifically linked to BT-R(1) in insect cells should provide insights into how insects evolve resistance to Bt and into the development of new, safer insecticides.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: Visualization
                Role: Formal analysisRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: Formal analysis
                Role: Formal analysis
                Role: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                13 December 2017
                2017
                : 12
                : 12
                : e0189214
                Affiliations
                [1 ] School of Horticulture and Plant Protection, Yangzhou University, Yangzhou P.R. China
                [2 ] Division of Plant Sciences, University of Missouri, Columbia, MO, United States of America
                [3 ] USDA/Agricultural Research Service, Biological Control of Insects Research Laboratory, Columbia, Missouri, 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.

                ‡ These authors are co-first authors on this work.

                Author information
                http://orcid.org/0000-0002-8539-9182
                Article
                PONE-D-17-18252
                10.1371/journal.pone.0189214
                5728565
                29236776
                ef1caa39-c61a-41f3-9a98-92fe31b10515
                © 2017 Ge 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
                : 11 May 2017
                : 21 November 2017
                Page count
                Figures: 6, Tables: 1, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 2017YFD0200400
                Award Recipient :
                Funded by: the project of Jiangsu Natural Science Foundation of China
                Award ID: BK20171283
                Award Recipient :
                Funded by: the Science and Technology innovation of Foundation of Yangzhou University
                Award ID: 2016CXJ065
                Award Recipient :
                Funded by: the Natural Science Foundation of China
                Award ID: (31201507)
                Award Recipient :
                Funded by: the Jiangsu Agricultural Scientific Self-innovation Fundation
                Award ID: CX(15)1057
                Award Recipient :
                Funded by: the Fundation of Science and Technology of Jiangsu Province, People’s Republic of China
                Award ID: BE2015342
                Award Recipient :
                This work was co-financed by National Key R & D Program of China (2017YFD0200400), the Natural Science Foundation of Jiangsu Province, China (BK20171283), the Science and Technology Innovation Foundation of Yangzhou University (2016CXJ065), the Natural Science Foundation of China (31201507), the Jiangsu Agricultural Scientific Self-innovation Foundation (CX(15)1057), and the Foundation of Science and Technology of Jiangsu Province, People’s Republic of China (BE2015342). 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
                Physiology
                Physiological Parameters
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Biology and Life Sciences
                Biochemistry
                Lipids
                Fats
                Biology and Life Sciences
                Anatomy
                Reproductive System
                Ovaries
                Medicine and Health Sciences
                Anatomy
                Reproductive System
                Ovaries
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Agriculture
                Pests
                Insect Pests
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Rice
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
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                Biology and Life Sciences
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                Body Weight
                Medicine and Health Sciences
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                Physiological Parameters
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