Chromosome-level genome assembly defines female-biased genes associated with sex determination and differentiation in the human blood fluke Schistosoma japonicum

Xindong Xu, Yifeng Wang, Changhong Wang, Gangqiang Guo, Xinyu Yu, Yang Dai, Yaobao Liu, Guiying Wei, Xiaohui He, Jin Ge, Ziqiu Zhang, Qingtian Guan, Arnab Pain, Shengyue Wang, Wenbao Zhang, Neil D. Young, Robin B. Gasser, Donald P. McManus, Jun Cao, Qi ZhouQingfeng Zhang

Research output: Contribution to journalArticlepeer-review

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 known for Schistosoma japonicum, the causative agent of schistosomiasis japonica. This mainly reflects the lack of high-quality genomic and transcriptomic resources for this species. As current genomes for S. japonicum are highly fragmented, we assembled and report 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 five and two evolutionary strata, respectively. By exploring the W-chromosome and sex-specific transcriptomes, we identified 35 W-linked genes and 257 female-preferentially transcribed genes (FTGs) from our chromosomal assembly and uncovered a signature for sex determination and differentiation in S. japonicum. These FTGs clustering within autosomes or the Z-chromosome exhibit a highly dynamic transcription profile during the pairing of female and male schistosomula, thereby representing a critical phase for the maturation of the female worms and suggesting distinct layers of regulatory control of gene transcription at this development stage. 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.
Original languageEnglish (US)
JournalMolecular Ecology Resources
DOIs
StatePublished - Jul 17 2022

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Biotechnology

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