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Chromosome-level genome assembly reveals female-biased genes for sex determination and differentiation in the human blood fluke Schistosoma japonicum
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  • Xindong Xu,
  • Yifeng Wang,
  • Qingtian Guan,
  • Gangqiang Guo,
  • Xinyu Yu,
  • Yang Dai,
  • Yaobao Liu,
  • Guiying Wei,
  • Changhong Wang,
  • Xiaohui He,
  • Jin Ge,
  • Ziqiu Zhang,
  • Arnab Pain,
  • Shengyue Wang,
  • Wenbao Wang,
  • Neil D. Young,
  • Robin Gasser,
  • Donald P. McManus,
  • Jun Cao,
  • Qi Zhou,
  • Qingfeng ZHANG
Xindong Xu
Tongji University

Corresponding Author:[email protected]

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Yifeng Wang
Zhejiang University
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Qingtian Guan
King Abdullah University of Science and Technology
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Gangqiang Guo
Tongji University
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Xinyu Yu
Jiangsu Institute of Parasitic Diseases
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Yang Dai
Jiangsu Institute of Parasitic Diseases
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Yaobao Liu
Jiangsu Institute of Parasitic Diseases
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Guiying Wei
Tongji University
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Changhong Wang
Tongji University
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Xiaohui He
Tongji University
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Jin Ge
Novogene Bioinformatics Institute
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Ziqiu Zhang
Novogene Bioinformatics Institute
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Arnab Pain
King Abdullah University of Science and Technology Biological and Environmental Science and Engineering Division
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Shengyue Wang
Shanghai Jiao Tong University
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Wenbao Wang
Xin Jiang Medical University
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Neil D. Young
The University of Melbourne
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Robin Gasser
The University of Melbourne
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Donald P. McManus
QIMR Berghofer Medical Research Institute
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Jun Cao
Jiangsu Institute of Parasitic Diseases
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Qi Zhou
Zhejiang University
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Qingfeng ZHANG
Tongji University
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Abstract

Schistosomiasis is a neglected tropical disease of humans caused by blood flukes of the genus Schistosoma – the only dioecious parasitic flatworms. Although aspects of sex determination, differentiation and reproduction have been studied in some Schistosoma species, almost nothing is understood for Schistosoma japonicum - the causative agent of schistosomiasis japonica. This relates mainly to a lack of high-quality genomic and transcriptomic resources for this species. As current draft genomes for S. japonicum are highly fragmented, we assembled here a chromosome-level reference genome (seven autosomes, the Z-chromosome and partial W-chromosome), achieving a substantially enhanced gene annotation. Utilising this genome, we discovered that the sex chromosomes of S. japonicum and its congener S. mansoni independently suppressed recombination during evolution, forming four and two ‘strata’, respectively. By exploring the W-chromosome and sex-specific transcriptomes, we identified 35 W-linked genes and 257 female-preferentially transcribed genes (FTGs) and identified a signature for sex determination and differentiation in S. japonicum. These FTGs cluster within autosomes or the Z-chromosome and exhibit a highly dynamic transcription profile during the pairing of female and male schistosomules (advanced juveniles), representing a critical phase for the maturation of the female worms, suggesting distinct layers of regulatory control of gene transcription at this stage of development. Collectively, these data provide a valuable resource for further functional genomic characterisation of S. japonicum, shed light on the evolution of sex chromosomes in this highly virulent human blood fluke and provide a pathway to identify novel targets for development of intervention tools against schistosomiasis.
10 Oct 2021Submitted to Molecular Ecology Resources
02 Nov 2021Submission Checks Completed
02 Nov 2021Assigned to Editor
07 Nov 2021Reviewer(s) Assigned
14 Jan 2022Review(s) Completed, Editorial Evaluation Pending
17 Jan 2022Editorial Decision: Revise Minor
11 Feb 2022Review(s) Completed, Editorial Evaluation Pending
11 Feb 20221st Revision Received
12 Feb 2022Reviewer(s) Assigned
13 Apr 2022Editorial Decision: Revise Minor
07 Jun 2022Review(s) Completed, Editorial Evaluation Pending
07 Jun 20222nd Revision Received
10 Jun 2022Editorial Decision: Revise Minor
05 Jul 20223rd Revision Received
05 Jul 2022Review(s) Completed, Editorial Evaluation Pending
11 Jul 2022Editorial Decision: Accept