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      Regulation of the Larval Transcriptome of Diatraea saccharalis (Lepidoptera: Crambidae) by Maternal and Other Factors of the Parasitoid Cotesia flavipes (Hymenoptera: Braconidae)

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          Abstract

          Koinobiont endoparasitoid wasps regulate the host’s physiology to their own benefit during their growth and development, using maternal, immature and/or derived-tissue weaponry. The tools used to subdue the wasps’ hosts interfere directly with host transcription activity. The broad range of host tissues and pathways affected impedes our overall understanding of the host-regulation process during parasitoid development. Next-generation sequencing and de novo transcriptomes are helpful approaches to broad questions, including in non-model organisms. In the present study, we used Illumina sequencing to assemble a de novo reference transcriptome of the sugarcane borer Diatraea saccharalis, to investigate the regulation of host gene expression by the larval endoparasitoid Cotesia flavipes. We obtained 174,809,358 reads and assembled 144,116 transcripts, of which 44,325 were putatively identified as lepidopteran genes and represented a substantial number of pathways that are well described in other lepidopteran species. Comparative transcriptome analyses of unparasitized versus parasitized larvae identified 1,432 transcripts of D. saccharalis that were up-regulated under parasitization by C. flavipes, while 1,027 transcripts were down-regulated. Comparison of the transcriptomes of unparasitized and pseudoparasitized D. saccharalis larvae led to the identification of 1,253 up-regulated transcripts and 972 down-regulated transcripts in the pseudoparasitized larvae. Analysis of the differentially expressed transcripts showed that C. flavipes regulated several pathways, including the Ca +2 transduction signaling pathway, glycolysis/gluconeogenesis, chitin metabolism, and hormone biosynthesis and degradation, as well as the immune system, allowing us to identify key target genes involved in the metabolism and development of D. saccharalis.

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          Calcium signaling.

          Calcium ions (Ca(2+)) impact nearly every aspect of cellular life. This review examines the principles of Ca(2+) signaling, from changes in protein conformations driven by Ca(2+) to the mechanisms that control Ca(2+) levels in the cytoplasm and organelles. Also discussed is the highly localized nature of Ca(2+)-mediated signal transduction and its specific roles in excitability, exocytosis, motility, apoptosis, and transcription.
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            The Toll and Imd pathways are the major regulators of the immune response in Drosophila.

            Microarray studies have shown recently that microbial infection leads to extensive changes in the Drosophila gene expression programme. However, little is known about the control of most of the fly immune-responsive genes, except for the antimicrobial peptide (AMP)-encoding genes, which are regulated by the Toll and Imd pathways. Here, we used oligonucleotide microarrays to monitor the effect of mutations affecting the Toll and Imd pathways on the expression programme induced by septic injury in Drosophila adults. We found that the Toll and Imd cascades control the majority of the genes regulated by microbial infection in addition to AMP genes and are involved in nearly all known Drosophila innate immune reactions. However, we identified some genes controlled by septic injury that are not affected in double mutant flies where both Toll and Imd pathways are defective, suggesting that other unidentified signalling cascades are activated by infection. Interestingly, we observed that some Drosophila immune-responsive genes are located in gene clusters, which often are transcriptionally co-regulated.
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              The Drosophila imd signaling pathway.

              The fruit fly, Drosophila melanogaster, has helped us to understand how innate immunity is activated. In addition to the Toll receptor and the Toll signaling pathway, the Drosophila immune response is regulated by another evolutionarily conserved signaling cascade, the immune deficiency (Imd) pathway, which activates NF-κB. In fact, the Imd pathway controls the expression of most of the antimicrobial peptides in Drosophila; thus, it is indispensable for normal immunity in flies. In this article, we review the current literature on the Drosophila Imd pathway, with special emphasis on its role in the (patho)physiology of different organs. We discuss the systemic response, as well as local responses, in the epithelial and mucosal surfaces and the nervous system.
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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
                06 September 2019
                2019
                : 10
                : 1106
                Affiliations
                Insect Interactions Laboratory, Department of Entomology and Acarology, College of Agriculture “Luiz de Queiroz”, University of São Paulo , Piracicaba, Brazil
                Author notes

                Edited by: Michel Cusson, Natural Resources Canada, Canada

                Reviewed by: Don Stoltz, Dalhousie University, Canada; M. Lukas Seehausen, CABI, Switzerland

                *Correspondence: Fernando Luis Cônsoli, fconsoli@ 123456usp.br

                ORCID: Fernando Luis Cônsoli orcid.org/0000-0002-2287-0782

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

                Article
                10.3389/fphys.2019.01106
                6742964
                31555143
                bbb3c09b-bfa7-4e12-9511-47bf3633650d
                Copyright © 2019 Merlin and Cônsoli.

                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
                : 04 January 2019
                : 12 August 2019
                Page count
                Figures: 7, Tables: 2, Equations: 0, References: 123, Pages: 19, Words: 0
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                calcium signaling regulation,gene expression,host regulation,host–parasitoid interactions,polydnavirus,sustainable pest management

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