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      Dynamic transcriptomes identify biogenic amines and insect-like hormonal regulation for mediating reproduction in Schistosoma japonicum

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          Abstract

          Eggs produced by the mature female parasite are responsible for the pathogenesis and transmission of schistosomiasis. Female schistosomes rely on a unique male-induced strategy to accomplish reproductive development, a process that is incompletely understood. Here we map detailed transcriptomic profiles of male and female Schistosoma japonicum across eight time points throughout the sexual developmental process from pairing to maturation. The dynamic gene expression pattern data reveal clear sex-related characteristics, indicative of an unambiguous functional division between males and females during their interplay. Cluster analysis, in situ hybridization and RNAi assays indicate that males likely use biogenic amine neurotransmitters through the nervous system to control and maintain pairing with females. In addition, the analyses indicate that reproductive development of females involves an insect-like hormonal regulation. These data sets and analyses serve as a foundation for deeper study of sexual development in this pathogen and identification of novel anti-schistosomal interventions.

          Abstract

          For reproduction, the human parasite Schistosoma japonicum relies on a complex and incompletely understood interplay between female and male schistosomes. Here the authors sequence the transcriptome of female and male schistosomes across eight time points during sexual development.

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          Most cited references64

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          De novo assembly and analysis of RNA-seq data.

          We describe Trans-ABySS, a de novo short-read transcriptome assembly and analysis pipeline that addresses variation in local read densities by assembling read substrings with varying stringencies and then merging the resulting contigs before analysis. Analyzing 7.4 gigabases of 50-base-pair paired-end Illumina reads from an adult mouse liver poly(A) RNA library, we identified known, new and alternative structures in expressed transcripts, and achieved high sensitivity and specificity relative to reference-based assembly methods.
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            Assessment of transcript reconstruction methods for RNA-seq

            RNA sequencing (RNA-seq) is transforming genome biology, enabling comprehensive transcriptome profiling with unprecendented accuracy and detail. Due to technical limitations of current high-throughput sequencing platforms, transcript identity, structure and expression level must be inferred programmatically from partial sequence reads of fragmented gene products. We evaluated 24 protocol variants of 14 independent computational methods for exon identification, transcript reconstruction and expression level quantification from RNA-seq data. Our results show that most algorithms are able to identify discrete transcript components with high success rates, but that assembly of complete isoform structures poses a major challenge even when all constituent elements are identified. Expression level estimates also varied widely across methods, even when based on similar transcript models. Consequently, the complexity of higher eukaryotic genomes imposes severe limitations in transcript recall and splice product discrimination that are likely to remain limiting factors for the analysis of current-generation RNA-seq data.
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              The Schistosoma japonicum genome reveals features of host-parasite interplay.

              (2009)
              Schistosoma japonicum is a parasitic flatworm that causes human schistosomiasis, which is a significant cause of morbidity in China and the Philippines. Here we present a draft genomic sequence for the worm. The genome provides a global insight into the molecular architecture and host interaction of this complex metazoan pathogen, revealing that it can exploit host nutrients, neuroendocrine hormones and signalling pathways for growth, development and maturation. Having a complex nervous system and a well-developed sensory system, S. japonicum can accept stimulation of the corresponding ligands as a physiological response to different environments, such as fresh water or the tissues of its intermediate and mammalian hosts. Numerous proteases, including cercarial elastase, are implicated in mammalian skin penetration and haemoglobin degradation. The genomic information will serve as a valuable platform to facilitate development of new interventions for schistosomiasis control.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                13 March 2017
                2017
                : 8
                : 14693
                Affiliations
                [1 ]State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center for Genetics and Development, School of Life Sciences, Fudan University , Shanghai 200438, China
                [2 ]Key Laboratory of Parasite and Vector Biology of the Chinese Ministry of Health, WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention , Shanghai 200025, China
                [3 ]Department of Microbiology, Immunology & Tropical Medicine, Research Center for the Neglected Diseases of Poverty, School of Medicine & Health Sciences, George Washington University , Washington DC 20037, USA
                [4 ]Molecular Parasitology Laboratory, Immunology Department, QIMR Berghofer Medical Research Institute , Brisbane, Queensland 4006, Australia
                Author notes
                [*]

                These authors contributed equally to this work

                Article
                ncomms14693
                10.1038/ncomms14693
                5355954
                28287085
                576e1108-007b-4abd-921d-f7e789aece2b
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 23 May 2016
                : 23 January 2017
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