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      Horizontal Transmission of Intracellular Insect Symbionts via Plants

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          Abstract

          Experimental evidence is accumulating that endosymbionts of phytophagous insects may transmit horizontally via plants. Intracellular symbionts known for manipulating insect reproduction and altering fitness ( Rickettsia, Cardinium, Wolbachia, and bacterial parasite of the leafhopper Euscelidius variegatus) have been found to travel from infected insects into plants. Other insects, either of the same or different species can acquire the symbiont from the plant through feeding, and in some cases transfer it to their progeny. These reports prompt many questions regarding how intracellular insect symbionts are delivered to plants and how they affect them. Are symbionts passively transported along the insect-plant-insect path, or do they actively participate in the process? How widespread are these interactions? How does symbiont presence influence the plant? And what conditions are required for the new infection to establish in an insect? From an ecological, evolutionary, and applied perspective, this mode of horizontal transmission could have profound implications if occurring frequently enough or if new stable symbiont infections are established. Transmission of symbionts through plants likely represents an underappreciated means of infection, both in terms of symbiont epidemiology and the movement of symbionts to new host species.

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          Most cited references55

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Role of phytohormones in insect-specific plant reactions.

            The capacity to perceive and respond is integral to biological immune systems, but to what extent can plants specifically recognize and respond to insects? Recent findings suggest that plants possess surveillance systems that are able to detect general patterns of cellular damage as well as highly specific herbivore-associated cues. The jasmonate (JA) pathway has emerged as the major signaling cassette that integrates information perceived at the plant-insect interface into broad-spectrum defense responses. Specificity can be achieved via JA-independent processes and spatio-temporal changes of JA-modulating hormones, including ethylene (ET), salicylic acid (SA), abscisic acid (ABA), auxin, cytokinins (CK), brassinosteroids (BR) and gibberellins (GB). The identification of receptors and ligands and an integrative view of hormone-mediated response systems are crucial to understand specificity in plant immunity to herbivores. Copyright © 2012 Elsevier Ltd. All rights reserved.
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              Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias.

              Maternally inherited bacterial symbionts of arthropods are common, yet symbiont invasions of host populations have rarely been observed. Here, we show that Rickettsia sp. nr. bellii swept into a population of an invasive agricultural pest, the sweet potato whitefly, Bemisia tabaci, in just 6 years. Compared with uninfected whiteflies, Rickettsia-infected whiteflies produced more offspring, had higher survival to adulthood, developed faster, and produced a higher proportion of daughters. The symbiont thus functions as both mutualist and reproductive manipulator. The observed increased performance and sex-ratio bias of infected whiteflies are sufficient to explain the spread of Rickettsia across the southwestern United States. Symbiont invasions such as this represent a sudden evolutionary shift for the host, with potentially large impacts on its ecology and invasiveness.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                28 November 2017
                2017
                : 8
                : 2237
                Affiliations
                [1] 1Department of Vector Biology, Max Planck Institute for Infection Biology , Berlin, Germany
                [2] 2Department of Entomology and Nematology, University of Florida , Gainesville, FL, United States
                [3] 3Institute of Integrative Biology, University of Liverpool , Liverpool, United Kingdom
                [4] 4Department of Pathology, Institute for Human Infections and Immunity, Center for Biodefense and Emerging Infectious Disease, Center for Tropical Diseases, University of Texas Medical Branch , Galveston, TX, United States
                Author notes

                Edited by: Michael Thomas-Poulsen, University of Copenhagen, Denmark

                Reviewed by: Łukasz Kajtoch, Institute of Systematics and Evolution of Animals (PAN), Poland; Enric Frago, Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), France

                *Correspondence: Ewa Chrostek, echrostek@ 123456gmail.com Grant L. Hughes, glhughes@ 123456utmb.edu

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02237
                5712413
                29234308
                2cf14728-f6fe-4e68-9a1f-e74085f741df
                Copyright © 2017 Chrostek, Pelz-Stelinski, Hurst and Hughes.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 08 August 2017
                : 31 October 2017
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 69, Pages: 8, Words: 0
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R21AI124452
                Award ID: R21AI12950701
                Funded by: Centers for Disease Control and Prevention 10.13039/100000030
                Award ID: U01CK000512
                Funded by: European Molecular Biology Organization 10.13039/100004410
                Award ID: EMBO ALTF 1497-2015
                Funded by: FP7 People: Marie-Curie Actions 10.13039/100011264
                Award ID: LTFCOFUND2013
                Award ID: GA-2013-609409
                Funded by: Natural Environment Research Council 10.13039/501100000270
                Award ID: NE/N010434/1
                Funded by: U.S. Department of Agriculture 10.13039/100000199
                Award ID: 00098869
                Categories
                Microbiology
                Mini Review

                Microbiology & Virology
                horizontal transmission,plant-mediated transmission,host-switching,plant-symbiont interaction,endosymbiont,wolbachia,rickettsia,cardinium

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