Chromatin structure changes around satellite repeats on the Schistosoma mansoni female sex chromosome suggest a possible mechanism for sex chromosome emergence

Abstract

BackgroundIn the leuphotrochozoan parasitic platyhelminth Schistosoma mansoni, male individuals are homogametic (ZZ) whereas females are heterogametic (ZW). To elucidate the mechanisms that led to the emergence of sex chromosomes, we compared the genomic sequence and the chromatin structure of male and female individuals. As for many eukaryotes, the lower estimate for the repeat content is 40%, with an unknown proportion of domesticated repeats. We used massive sequencing to de novo assemble all repeats, and identify unambiguously Z-specific, W-specific and pseudoautosomal regions of the S. mansoni sex chromosomes.ResultsWe show that 70 to 90% of S. mansoni W and Z are pseudoautosomal. No female-specific gene could be identified. Instead, the W-specific region is composed almost entirely of 36 satellite repeat families, of which 33 were previously unknown. Transcription and chromatin status of female-specific repeats are stage-specific: for those repeats that are transcribed, transcription is restricted to the larval stages lacking sexual dimorphism. In contrast, in the sexually dimorphic adult stage of the life cycle, no transcription occurs. In addition, the euchromatic character of histone modifications around the W-specific repeats decreases during the life cycle. Recombination repression occurs in this region even if homologous sequences are present on both the Z and W chromosomes.ConclusionOur study provides for the first time evidence for the hypothesis that, at least in organisms with a ZW type of sex chromosomes, repeat-induced chromatin structure changes could indeed be the initial event in sex chromosome emergence.

Efficient linkage mapping using exome capture and extreme QTL in schistosome parasites

“…The distribution of the read depth was similar between sexes except for parts of the Z chromosome in the females in which read depth is reduced by half (Table 1, Figure 2). These genome regions (position 3.5-19.5 Mb and 23.5-31 Mb) correspond to the heterochromatin domain of the W chromosome (female sex-specific chromosome) [31] and contain all the Z-specific markers of the genetic map of S. mansoni (data not shown) [22]. …”

“…These regions correspond exactly to those identified by Lepesant et al . and carrying W specific sequences [31], and also correspond to the positions of markers showing Z-linked inheritance patterns in the cross used to construct the genetic map [22]. …”

Whole genome amplification and exome sequencing of archived schistosome miracidia

“…Read depth was even across the exome (Figure 3), except in parts of the Z chromosome in S. mansoni females where read depth is halved (females are ZW). These genome regions (position 3.5–19.5 Mb and 23.5–31 Mb for S. mansoni (Lepesant et al 2012)) correspond to the non-recombining heterochromatin domain of the W chromosome. The read depth in the Z-linked region allows us to determine the parasite sex in silico using a read depth ratio between the Z-linked region and the rest of the chromosome.…”

The roles of Dmrt (Double sex/Male-abnormal-3 Related Transcription factor) genes in sex determination and differentiation mechanisms: Ubiquity and diversity across the animal kingdom

“…First, it could be interesting to analyze the role of these genes in an evolutionary young sex chromosome system, such as that of the Schistosoma Platyhelminth [95]. Second, studies on successive hermaphroditic organisms are also of great interest that has been shown in fishes or salamanders.…”