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      Gall Wasp Transcriptomes Unravel Potential Effectors Involved in Molecular Dialogues With Oak and Rose

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          Abstract

          To gain insight into wasp factors that might be involved in the initial induction of galls on woody plants, we performed high throughput (454) transcriptome analysis of ovaries and venom glands of two cynipid gall wasps, Biorhiza pallida and Diplolepis rosae, inducing galls on oak and rose, respectively. De novo assembled and annotated contigs were compared to sequences from phylogenetically related parasitoid wasps. The relative expression levels of contigs were estimated to identify the most expressed gene sequences in each tissue. We identify for the first time a set of maternally expressed gall wasp proteins potentially involved in the interaction with the plant. Some genes highly expressed in venom glands and ovaries may act to suppress early plant defense signaling. We also identify gall wasp cellulases that could be involved in observed local lysis of plant tissue following oviposition, and which may have been acquired from bacteria by horizontal gene transfer. We find no evidence of virus-related gene expression, in contrast to many non-cynipid parasitoid wasps. By exploring gall wasp effectors, this study is a first step toward understanding the molecular mechanisms underlying cynipid gall induction in woody plants, and the recent sequencing of oak and rose genomes will enable study of plant responses to these factors.

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          Most cited references79

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          Adaptive Nature of Insect Galls

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            Myrosinase: gene family evolution and herbivore defense in Brassicaceae.

            Glucosinolates are a category of secondary products present primarily in species of the order Capparales. When tissue is damaged, for example by herbivory, glucosinolates are degraded in a reaction catalyzed by thioglucosidases, denoted myrosinases, also present in these species. Thereby, toxic compounds such as nitriles, isothiocyanates, epithionitriles and thiocyanates are released. The glucosinolate-myrosinase system is generally believed to be part of the plant's defense against insects, and possibly also against pathogens. In this review, the evolution of the system and its impact on the interaction between plants and insects are discussed. Further, data suggesting additional functions in the defense against pathogens and in sulfur metabolism are reviewed.
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              Horizontal Gene Transfer Contributes to the Evolution of Arthropod Herbivory

              Within animals, evolutionary transition toward herbivory is severely limited by the hostile characteristics of plants. Arthropods have nonetheless counteracted many nutritional and defensive barriers imposed by plants and are currently considered as the most successful animal herbivores in terrestrial ecosystems. We gather a body of evidence showing that genomes of various plant feeding insects and mites possess genes whose presence can only be explained by horizontal gene transfer (HGT). HGT is the asexual transmission of genetic information between reproductively isolated species. Although HGT is known to have great adaptive significance in prokaryotes, its impact on eukaryotic evolution remains obscure. Here, we show that laterally transferred genes into arthropods underpin many adaptations to phytophagy, including efficient assimilation and detoxification of plant produced metabolites. Horizontally acquired genes and the traits they encode often functionally diversify within arthropod recipients, enabling the colonization of more host plant species and organs. We demonstrate that HGT can drive metazoan evolution by uncovering its prominent role in the adaptations of arthropods to exploit plants.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                24 July 2019
                2019
                : 10
                : 926
                Affiliations
                [1] 1UMR 7261 CNRS, Institut de Recherche sur la Biologie de l’Insecte, Faculté des Sciences et Techniques, Université de Tours , Tours, France
                [2] 2Institute of Evolutionary Biology, The University of Edinburgh , Edinburgh, United Kingdom
                Author notes

                Edited by: Patrizia Falabella, University of Basilicata, Italy

                Reviewed by: Sassan Asgari, The University of Queensland, Australia; Edward F. Connor, San Francisco State University, United States

                *Correspondence: Jean-Michel Drezen, drezen@ 123456univ-tours.fr

                Present address: Sébastien Cambier, Environmental Research and Innovation Department, Luxembourg Institute of Science and Technology, Esch-sur-Alzette, Luxembourg Jack Hearn, Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2019.00926
                6667641
                31396099
                3f3f30af-6a02-4de9-ad95-9b0505ecf676
                Copyright © 2019 Cambier, Ginis, Moreau, Gayral, Hearn, Stone, Giron, Huguet and Drezen.

                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) and the copyright owner(s) 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
                : 03 April 2019
                : 09 July 2019
                Page count
                Figures: 7, Tables: 4, Equations: 0, References: 86, Pages: 18, Words: 0
                Funding
                Funded by: Agence Nationale de la Recherche 10.13039/501100001665
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                oak gall wasp,rose gall wasp,gall induction,venom,ovary secretions
                Anatomy & Physiology
                oak gall wasp, rose gall wasp, gall induction, venom, ovary secretions

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