Schistosome sex matters: a deep view into gonad-specific and pairing-dependent transcriptomes reveals a complex gender interplay

Abstract

As a key event for maintaining life cycles, reproduction is a central part of platyhelminth biology. In case of parasitic platyhelminths, reproductive processes can also contribute to pathology. One representative example is the trematode Schistosoma, which causes schistosomiasis, an infectious disease, whose pathology is associated with egg production. Among the outstanding features of schistosomes is their dioecious lifestyle and the pairing-dependent differentiation of the female gonads which finally leads to egg synthesis. To analyze the reproductive biology of Schistosoma mansoni in-depth we isolated complete ovaries and testes from paired and unpaired schistosomes for comparative RNA-seq analyses. Of >7,000 transcripts found in the gonads, 243 (testes) and 3,600 (ovaries) occurred pairing-dependently. Besides the detection of genes transcribed preferentially or specifically in the gonads of both genders, we uncovered pairing-induced processes within the gonads including stem cell-associated and neural functions. Comparisons to work on neuropeptidergic signaling in planarian showed interesting parallels but also remarkable differences and highlights the importance of the nervous system for flatworm gonad differentiation. Finally, we postulated first functional hints for 235 hypothetical genes. Together, these results elucidate key aspects of flatworm reproductive biology and will be relevant for basic as well as applied, exploitable research aspects.

Serine/threonine protein phosphatase 1 (PP1) controls growth and reproduction in Schistosoma japonicum

“…This conclusion is strongly supported by the transcriptomic data. In addition to down-regulation of eggshell synthesis-associated genes in females, such as putative eggshell protein, trematode eggshell synthesis protein, and tyrosinases after Sj-pp1cs knockdown ( Table 1), stem cell and neoblast-associated genes such as fibroblast growth factor receptor (Sjp_ 0112660), argonaute-2 (Sjp_0045200), and nanos (Sjp_ 0060520) were also down-regulated (genes known to participate in gonadal stem cell activities) (24,54). Among these, fibroblast growth factor receptors are not only involved in regulation and maintenance of proliferating somatic cells but are also required for gonad differentiation and reproduction in S. mansoni (24,55).…”

(Epi)genetic Inheritance in Schistosoma mansoni: A Systems Approach

“…In addition to the host environment, both sexes depend on each other's microenvironment and mating status (i.e., paired versus unpaired) for the maturation of both male and female parasites [37]. A recent study has reinforced this observation of pairing-dependent transcriptome alterations and further demonstrated that about 4000 gonadal expressed genes are regulated by the presence of the opposite gender [38]. The maturation process is reversible when individuals are separated for sufficiently long time.…”

Genetic dissection of the planarian reproductive system through characterization of Schmidtea mediterranea CPEB homologs

“…Expression of Cytoplasmic Polyadenylation Element Binding protein (CPEB) homologs has been detected recently in the germline of the fluke Schistosoma mansoni and the non-parasitic flatworm Macrostomum lignano (Arbore et al, 2015; Cogswell et al, 2012; Lu et al, 2016). Members of the CPEB family of proteins are key regulators of mRNA during metazoan germline development.…”