Oocyte-somatic cells interactions, lessons from evolution

Abstract

Background: Despite the known importance of somatic cells for oocyte developmental competence acquisition, the overall mechanisms underlying the acquisition of full developmental competence are far from being understood, especially in non-mammalian species. The present work aimed at identifying key molecular signals from somatic origin that would be shared by vertebrates.

Results: Using a parallel transcriptomic analysis in 4 vertebrate species - a teleost fish, an amphibian, and two mammals - at similar key steps of developmental competence acquisition, we identified a large number of species-specific differentially expressed genes and a surprisingly high number of orthologous genes exhibiting similar expression profiles in the 3 tetrapods and in the 4 vertebrates. Among the evolutionary conserved players participating in developmental competence acquisition are genes involved in key processes such as cellular energy metabolism, cell-to-cell communications, and meiosis control. In addition, we report many novel molecular actors from somatic origin that have never been studied in the vertebrate ovary. Interestingly, a significant number of these new players actively participate in Drosophila oogenesis.

Conclusions: Our study provides a comprehensive overview of evolutionary-conserved mechanisms from somatic origin participating in oocyte developmental competence acquisition in 4 vertebrates. Together our results indicate that despite major differences in ovarian follicular structure, some of the key players from somatic origin involved in oocyte developmental competence acquisition would be shared, not only by vertebrates, but also by metazoans. The conservation of these mechanisms during vertebrate evolution further emphasizes the important contribution of the somatic compartment to oocyte quality and paves the way for future investigations aiming at better understanding what makes a good egg.

Figure 1

Differentially expressed orthologous genes exhibiting a conserved expression profile in rainbow trout and Xenopus. (A) Supervised clustering of expression profiles in the somatic layers of the ovarian follicle in rainbow trout and Xenopus during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2). For each species, the number of differentially expressed orthologous genes is indicated. (B) The expression profiles of specific genes are shown.

Figure 2

Differentially expressed orthologous genes exhibiting a conserved expression profile in mouse and cow. (A) Supervised clustering of expression profiles in the somatic layers of the ovarian follicle in mouse and cow species during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2). For each species, the number of differentially expressed orthologous genes is indicated. (B) Gene ontology and KEGG pathways enrichment score in clusters 1 and 2. Stars denote the p-values: * p<0.05; ** p<0.01; *** p<0.001.

Figure 3

Differentially expressed orthologous genes exhibiting a conserved expression profile in Xenopus, mouse, and cow. (A) Supervised clustering of expression profiles in the somatic layers of the ovarian follicle in Xenopus, mouse, and cow species during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2). For each species, the number of differentially expressed orthologous genes is indicated. (B) Gene ontology and KEGG pathways enrichment score. Stars denote the p-values: * p<0.05; ** p<0.01; *** p<0.001.

Figure 4

Expression profiles of specific orthologous genes in Xenopus, mouse, and cow. The microarray expression profiles of specific gene in the somatic cells surrounding the oocyte during competence acquisition are shown. The mean expression is shown for the following: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2).

Figure 5

Differentially expressed orthologous genes exhibiting a conserved expression profile in rainbow trout, Xenopus, mouse, and cow. A. Supervised clustering of expression profiles in the somatic layers of the ovarian follicle in rainbow trout, Xenopus, mouse, and cow species during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2). For each species, the number of differentially expressed orthologous genes is indicated. B. Gene ontology enrichment score in clusters 1 and 2 (p<0.05).

Figure 6

Conserved expression profiles of genes of the Klhl gene family in somatic follicular cells during oocyte developmental competence acquisition. Expression profiles in the somatic layers of the ovarian follicle in the 4 species during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2).

Figure 7

Conserved expression profiles of Adamts1 and Klf13 genes in somatic follicular cells during oocyte developmental competence acquisition. Expression profiles in the somatic layers of the ovarian follicle in the 4 species during oocyte developmental competence acquisition: developmentally incompetent or poorly competent prophase I oocytes (NC1), developmentally competent prophase I oocytes (C1), and developmentally competent metaphase II oocytes (C2).