Chromosome-level genome assembly reveals female-biased genes for sex
determination and differentiation in the human blood fluke Schistosoma
japonicum
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.