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      Collembolan Transcriptomes Highlight Molecular Evolution of Hexapods and Provide Clues on the Adaptation to Terrestrial Life

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          Abstract

          Background

          Collembola (springtails) represent a soil-living lineage of hexapods in between insects and crustaceans. Consequently, their genomes may hold key information on the early processes leading to evolution of Hexapoda from a crustacean ancestor.

          Method

          We assembled and annotated transcriptomes of the Collembola Folsomia candida and Orchesella cincta, and performed comparative analysis with protein-coding gene sequences of three crustaceans and three insects to identify adaptive signatures associated with the evolution of hexapods within the pancrustacean clade.

          Results

          Assembly of the springtail transcriptomes resulted in 37,730 transcripts with predicted open reading frames for F. candida and 32,154 for O. cincta, of which 34.2% were functionally annotated for F. candida and 38.4% for O. cincta. Subsequently, we predicted orthologous clusters among eight species and applied the branch-site test to detect episodic positive selection in the Hexapoda and Collembola lineages. A subset of 250 genes showed significant positive selection along the Hexapoda branch and 57 in the Collembola lineage. Gene Ontology categories enriched in these genes include metabolism, stress response (i.e. DNA repair, immune response), ion transport, ATP metabolism, regulation and development-related processes (i.e. eye development, neurological development).

          Conclusions

          We suggest that the identified gene families represent processes that have played a key role in the divergence of hexapods within the pancrustacean clade that eventually evolved into the most species-rich group of all animals, the hexapods. Furthermore, some adaptive signatures in collembolans may provide valuable clues to understand evolution of hexapods on land.

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          Most cited references57

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          Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology.

          Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
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            Evolution of genes and genomes on the Drosophila phylogeny.

            Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.
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              The genome of the model beetle and pest Tribolium castaneum.

              Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                15 June 2015
                2015
                : 10
                : 6
                : e0130600
                Affiliations
                [1 ]Department of Ecological Science, VU University Amsterdam, Amsterdam, The Netherlands
                [2 ]EMBL-European Bioinformatics Institute, Cambridge, United Kingdom
                [3 ]Microarray Facility, VU Medical Center, Amsterdam, The Netherlands
                [4 ]Department of Microbiology, Radboud University Nijmegen, Nijmegen, The Netherlands
                [5 ]Keygene NV, Wageningen, The Netherlands
                [6 ]Leiden Genome Technology Center, Human and Clinical Genetics, Leiden University Medical Center, Leiden, The Netherlands
                Max F. Perutz Laboratories, AUSTRIA
                Author notes

                Competing Interests: One of the authors has an affiliation to Keygene NV. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: AF DR NMvS. Performed the experiments: DR JM JTdD KK. Analyzed the data: AF DS BY HJModC ED RAS. Wrote the paper: AF DR NMvS RAS KK DS BY JM HJModC ED JTdD.

                Article
                PONE-D-15-07505
                10.1371/journal.pone.0130600
                4468109
                26075903
                ca37ef74-efa3-4a68-b58e-ac3327a24540
                Copyright @ 2015

                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
                : 18 February 2015
                : 21 May 2015
                Page count
                Figures: 3, Tables: 1, Pages: 18
                Funding
                This research was supported by a grant from the Dutch Biotechnology based Ecologically Balanced Sustainable Industrial Consortium (BE-BASIC), grant number F08.001.03, http://www.be-basic.org. In addition, D. Roelofs is supported by the European Union FP7 large scale intergration Project ‘Sustainable Nanotechnologies (SUN)’, Grant number 604305. Keygene NV provided support in the form of salaries for E. Datema, but did not have any additional role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                The sequencing data is deposited to NCBI’s Sequence Read Archive (SRA) under accessions SRR935329 and SRR935330. Assembled transcriptomes are submitted to NCBI transcriptome shotgun assembly database (TSA) under BioProject No. PRJNA211850 and PRJNA211851.

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