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Comparative Study
. 2018 Oct 1;10(10):2629-2642.
doi: 10.1093/gbe/evy158.

Genes Involved in Drosophila Melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

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Free PMC article
Comparative Study

Genes Involved in Drosophila Melanogaster Ovarian Function Are Highly Conserved Throughout Evolution

Sebastien Elis et al. Genome Biol Evol. .
Free PMC article

Abstract

This work presents a systematic approach to study the conservation of genes between fruit flies and mammals. We have listed 971 Drosophila genes involved in female reproduction at the ovarian level and systematically looked for orthologs in the Ciona, zebrafish, coelacanth, lizard, chicken, and mouse. Depending on the species, the percentage of these Drosophila genes with at least one ortholog varies between 69% and 78%. In comparison, only 42% of all the Drosophila genes have an ortholog in the mouse genome (P < 0.0001), suggesting a dramatically higher evolutionary conservation of ovarian genes. The 177 Drosophila genes that have no ortholog in mice and other vertebrates correspond to genes that are involved in mechanisms of oogenesis that are specific to the fruit fly or the insects. Among 759 genes with at least one ortholog in the zebrafish, 73 have an expression enriched in the ovary in this species (RNA-seq data). Among 760 genes that have at least one ortholog in the mouse; 76 and 11 orthologs are reported to be preferentially and exclusively expressed in the mouse ovary, respectively (based on the UniGene expressed sequence tag database). Several of them are already known to play a key role in murine oogenesis and/or to be enriched in the mouse/zebrafish oocyte, whereas others have remained unreported. We have investigated, by RNA-seq and real-time quantitative PCR, the exclusive ovarian expression of 10 genes in fish and mammals. Overall, we have found several novel candidates potentially involved in mammalian oogenesis by an evolutionary approach and using the fruit fly as an animal model.

Figures

Fig. 1.
Fig. 1.
Drosophila genes possessing a chordate orthologous gene. Number and percentage of orthologs of the 971 Drosophila melanogaster genes and of the complete Drosophila gene repertoire were obtained for each species considered using the Ensembl metazoa gene and Ensembl gene databases and the BioMart tool, as described in Materials and Methods section. Comparison of ortholog percentage of the 971 selected genes and the Drosophila gene repertoire were performed using χ2 tests. *Significant difference (P < 0.0001).
Fig. 2.
Fig. 2.
—Biological process GO enrichment. Fold enrichment of biological process GO in either zebrafish or mouse ortholog genes compared with the 971 Drosophila genes. GO analyses were performed using DAVID 6.8 (https://david.ncifcrf.gov/home.jsp). Only significantly enriched biological processes were represented (P < 0.05, Bonferroni corrected).
Fig. 3.
Fig. 3.
—Molecular function GO enrichment. Fold enrichment of molecular function GO in either zebrafish or mouse ortholog genes compared with the 971 Drosophila genes. GO analyses were performed using DAVID 6.8 (https://david.ncifcrf.gov/home.jsp). Only significantly enriched molecular functions were represented (P < 0.05, Bonferroni corrected).
Fig. 4.
Fig. 4.
Drosophila genes possessing no chordate orthologous gene. Number and percentage of orthologs of the 178 Drosophila melanogaster genes exhibiting no ortholog genes in chordates were obtained for each species considered using the Ensembl metazoa gene and Ensembl gene databases and the BioMart tool, as described in Materials and Methods section. Comparison of ortholog percentages of the selected 178 genes and the Drosophila gene repertoire were performed using χ2 tests. *Significant difference (P < 0.0001).
Fig. 5.
Fig. 5.
—Biological process GO enrichment in ovarian genes. Fold enrichment of biological process GO in mouse ortholog genes exhibiting an ovarian expression compared with the complete list of mouse ortholog genes (1,556 genes). Fold enrichment of biological process GO in zebrafish ortholog genes exhibiting an ovarian expression compared with the complete list of zebrafish ortholog genes (1,849 genes). GO analyses were performed using DAVID 6.8 (https://david.ncifcrf.gov/home.jsp). Only significantly enriched biological processes were represented (P < 0.05, raw P values).
Fig. 6.
Fig. 6.
—Gene expression in mouse tissues. Expression of 11 candidate genes was assessed in 10 mouse tissues (O, ovary; T, testis; M, muscle; U, uterus; Li, liver; S, spleen; B, brain; K, kidney; Bl, bladder and H, heart). After mRNA extraction and RT, qPCR was performed on tissues of three females or males. Expression of candidate genes is normalized by the expression of the Rpl19 housekeeping gene and presented as mean±SEM of three replicates. Different letters indicate a significant difference (P < 0.05). Therefore, if, at least, one letter is common between conditions, there is no significant difference between these two conditions (e.g., a is different from b but ab is not different from b. . .).
Fig. 7.
Fig. 7.
—Gene expression in medaka tissues. Expression of 7 candidate genes was assessed in 10 medaka tissues (O, ovary; T, testis; M, muscle; L, liver; B, brain; K, kidney; I, intestine; E, eye; G, gills and F, fins). After mRNA extraction and RT, qPCR was performed on tissues of eight females or males. Expression of candidate genes is normalized using exogenous luciferase transcript abundance in samples and presented as mean±SEM of eight replicates. Different letters indicate a significant difference (P < 0.05). Therefore, if, at least, one letter is common between conditions, there is no significant difference between these two conditions (e.g., a is different from b but ab is not different from b. . .).

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