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Bioinformatic analysis of female-specific, repetitive sequences  

Exceptional within the phylum Plathelminthes is the genus Schistosoma, which covers species exhibiting sexual dimorphism at the adult stage. It has long been of great interest to detect female-specific sequences and to analyze their function1-3. Genetically, the sexes differ e.g. in their karyotype, females have one W and one Z chromosome, males in contrast have two Z chromosomes. Large parts of the Z and W chromosomes are identical. However, there is a large heterochromatic area on the W chromosome, which does not appear on the Z chromosome, and which has been considered as female-specific. In previous studies, repetitive sequences in S. mansoni were detected in the heterochromatic region of the W chromosome and declared as female-specific W elements1-3. However, later studies revealed that these W elements can also occur in males. This led to the assumption of illegitimate recombination processes4,5. Furthermore, the possibility was discussed that these sequences are transcribed6, have a mobile, transposon-like character7 and are involved in the evolution of sex chromosomes8.

In this project, we intend to further investigate the phenomenon of mobile W elements. Therefore, W elements will be bioinformatically analyzed in the context of genome and transcriptome analyses9-12. The aim is to characterize W elements with respect to their group memberships, their activities in different stages of the life cycle of S. mansoni (Fig. 1) and additionally on a structural basis (Fig. 2) in order to get clues about their mobile behavior and their possible function.  



Fig. 1: Exemplary presentation of examined RNA-Seq data sets in the Genome Browser (IGV)13,14 to analyze transcript profiles of W-elements. The bars indicate transcripts of one W-element, which occurs in the respective RNA-Seq data set. The repetitive character of this W-element can be recognized by the repeated bar pattern. There are significant differences between the different samples with regard to transcript occurrence. In ovaries of unpaired females (sO1), a high level of transcripts of this W-element was detected, significantly more than in ovaries of paired females (bO1). In testes of unpaired males (sT1), transcripts were found in contrast to testes of paired males (bT1). In cercariae, transcript amounts in both sexes were almost identical (Mcer1, Fcer1; M=male, F=female, cer=cercariae).  


Fig. 2: Dotplot diagram (left) and enlarged areas (center, right) to investigate W-elements in S. mansoni. In this analysis, a sequence is compared to itself in order to identify specific patterns within the sequence. Outside the main diagonal, repetitive units appear as lines. In this example, a 403 bp long sequence occuring 101 times on the W chromosome was detected. The graphic was generated using the program Gepard V. 1.4015.  


1Spotila LD, Rekosh DM, Boucher JM, LoVerde PT (1987) A cloned DNA probe identifies the sex of Schistosoma mansoni cercariae. Molecular and Biochemical Parasitology 26:17–20. doi:10.1016/0166-6851(87)90125-3

2Webster P, Mansour TE, Bieber D (1989) Isolation of a female-specific, highly repeated Schistosoma mansoni DNA probe and its use in an assay of cercarial sex. Molecular and Biochemical Parasitology 36:217–222. doi:10.1016/0166-6851(89)90169-2

3Drew AC, Brindley PJ (1995) Female-specific sequences isolated from Schistosoma mansoni by representational difference analysis. Molecular and Biochemical Parasitology 71:173–181. doi:10.1016/0166-6851(95)00048-6

4Grevelding CG (1995) The female-specific W1 sequence of the Puerto Rican strain of Schistosoma mansoni occurs in both genders of a Liberian strain. Molecular and Biochemical Parasitology 71:269–272. doi:10.1016/0166-6851(94)00058-u

5Quack T, Doenhoff M, Kunz W, Grevelding CG (1998) Schistosoma mansoni; The varying occurrence of repetitive elements in different strains shows sex-specific polymorphisms. Experimental Parasitology 89:222–227. doi:10.1006/expr.1998.4293

6Fitzpatrick JM, Johnston DA, Williams GW, Williams DJ, Freeman TC, Dunne DW, Hoffmann KF (2005) An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Molecular and Biochemical Parasitology 141:1–13. doi:10.1016/j.molbiopara.2005.01.007

7Grevelding CG (1999) Genomic instability in Schistosoma mansoni. MolBiochemParasitol 101(1-2): 207-216

8Lepesant JMJ, Cosseau C, Boissier J, Freitag M, Portela J, Climent D, Perrin C, Zerlotini A, Grunau C (2012) Chromatin structural changes around satellite repeats on the female sex chromosome in Schistosoma mansoni and their possible role in sex chromosome emergence. Genome Biology 13:R14. doi:10.1186/gb-2012-13-2-r14

9Lu Z, Sessler F, Holroyd N, Hahnel S, Quack T, Berriman M, Grevelding CG (2016) Schistosome sex matters; A deep view into gonad-specific and pairing-dependent transcriptomes reveals a complex gender interplay. Scientific Reports 6:31150 EP -. doi:10.1038/srep31150

10Picard MAL, Boissier J, Roquis D, Grunau C, Allienne J-F, Duval D, Toulza E, Arancibia N, Caffrey CR, Long T, Nidelet S, Rohmer M, Cosseau C (2016) Sex-biased transcriptome of Schistosoma mansoni; Host-parasite interaction, genetic determinants and epigenetic regulators are associated with sexual differentiation. PLoS Neglected Tropical Diseases 10:e0004930. doi:10.1371/journal.pntd.0004930

11Protasio AV, Tsai IJ, Babbage A, Nichol S, Hunt M, Aslett MA, Silva N de, Velarde GS, Anderson TJC, Clark RC, Davidson C, Dillon GP, Holroyd NE, LoVerde PT, Lloyd C, McQuillan J, Oliveira G, Otto TD, Parker-Manuel SJ, Quail MA, Wilson RA, Zerlotini A, Dunne DW, Berriman M (2012) A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni.PLoS Neglected Tropical Diseases 6:e1455. doi:10.1371/journal.pntd.0001455

12Wang B, Collins JJ, Newmark PA (2013) Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni. eLife 2:e00768. doi:10.7554/eLife.00768

13James T. Robinson, Helga Thorvaldsdóttir, Wendy Winckler, Mitchell Guttman, Eric S. Lander, Gad Getz, Jill P. Mesirov. Integrative Genomics Viewer. Nature Biotechnology 29, 24–26 (2011)

14Helga Thorvaldsdóttir, James T. Robinson, Jill P. Mesirov. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 14, 178-192 (2013).

15Krumsiek J, Arnold R, Rattei T. Gepard: A rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 2007; 23(8): 1026-8. PMID: 17309896