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Diversification of MIF immune regulators in aphids: link with agonistic and antagonistic interactions

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      Abstract

      Background

      The widespread use of genome sequencing provided evidences for the high degree of conservation in innate immunity signalling pathways across animal phyla. However, the functioning and evolutionary history of immune-related genes remains unknown for most invertebrate species. A striking observation coming from the analysis of the pea aphid Acyrthosiphon pisum genome is the absence of important conserved genes known to be involved in the antimicrobial responses of other insects. This reduction in antibacterial immune defences is thought to be related to their long-term association with beneficial symbiotic bacteria and to facilitate symbiont maintenance. An additional possibility to avoid elimination of mutualistic symbionts is a fine-tuning of the host immune response. To explore this hypothesis we investigated the existence and potential involvement of immune regulators in aphid agonistic and antagonistic interactions.

      Results

      In contrast to the limited antibacterial arsenal, we showed that the pea aphid Acyrthosiphon pisum expresses 5 members of Macrophage Migration Inhibitory Factors (ApMIF), known to be key regulators of the innate immune response. In silico searches for MIF members in insect genomes followed by phylogenetic reconstruction suggest that evolution of MIF genes in hemipteran species has been shaped both by differential losses and serial duplications, raising the question of the functional importance of these genes in aphid immune responses. Expression analyses of ApMIFs revealed reduced expression levels in the presence, or during the establishment of secondary symbionts. By contrast, ApMIFs expression levels significantly increased upon challenge with a parasitoid or a Gram-negative bacteria. This increased expression in the presence of a pathogen/parasitoid was reduced or missing, in the presence of facultative symbiotic bacteria.

      Conclusions

      This work provides evidence that while aphid’s antibacterial arsenal is reduced, other immune genes widely absent from insect genomes are present, diversified and differentially regulated during antagonistic or agonistic interactions.

      Electronic supplementary material

      The online version of this article (doi:10.1186/1471-2164-15-762) contains supplementary material, which is available to authorized users.

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      Most cited references 51

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            Author and article information

            Affiliations
            [ ]Sophia Agrobiotech Institute, INRA-CNRS-UNS, UMR 7254, 400 Route des Chappes, 06 903 Sophia Antipolis, France
            [ ]Institut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS/Université François-Rabelais, Parc Grandmont, 37200 Tours, France
            [ ]Institute of Genetics, Environment and Plant Protection, INRA, UMR 1349, Domaine de la Motte, BP 35327, 35653 Le Rheu Cedex, France
            Contributors
            geraldine.dubreuil@univ-tours.fr
            emeline.deleury@sophia.inra.fr
            didier.crochard@sophia.inra.fr
            jean-christophe.simon@rennes.inra.fr
            Christine.coustau@sophia.inra.fr
            Journal
            BMC Genomics
            BMC Genomics
            BMC Genomics
            BioMed Central (London )
            1471-2164
            5 September 2014
            5 September 2014
            2014
            : 15
            : 1
            25193628
            4169804
            6457
            10.1186/1471-2164-15-762
            © Dubreuil et al.; licensee BioMed Central Ltd. 2014

            This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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            Research Article
            Custom metadata
            © The Author(s) 2014

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