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, 20 (1), 315

Postovulatory Maternal Transcriptome in Atlantic Salmon and Its Relation to Developmental Potential of Embryos

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Postovulatory Maternal Transcriptome in Atlantic Salmon and Its Relation to Developmental Potential of Embryos

Teshome Tilahun Bizuayehu et al. BMC Genomics.

Abstract

Background: Early development of an oviparous organism is based on maternally stocked structural, nutritional and regulatory components. These components influence the future developmental potential of an embryo, which is referred to as egg quality. Until zygotic genome activation, translational activity in a fish early embryo is limited to parentally inherited transcripts only. In this study, we asked whether egg transcriptome is associated with egg quality in Atlantic salmon (Salmo salar), which is capable of storing ovulated eggs in its abdominal cavity for a long time before spawning.

Results: We analyzed messenger RNA (mRNA) and micro RNA (miRNA) transcriptomes throughout the post-ovulatory egg retention period in batches of eggs from two quality groups, good and poor, classified based on the future developmental performance. We identified 28,551 protein-coding genes and 125 microRNA families, with 200 mRNAs and 5 miRNAs showing differential abundance between egg quality groups and/or among postovulatory ages. Transcriptome dynamics during the egg retention period was different in the two egg quality groups. We identified only a single gene, hepcidin-1, as a potential marker for Atlantic salmon egg quality evaluation.

Conclusion: The overlapping effect of post-ovulatory age on intrinsic egg developmental competence makes the quantification of egg quality difficult when based on transcripts abundance only.

Keywords: Atlantic salmon; Egg quality; Hepcidin-1; Maternal factors; Postovulatory aging; RNA-seq; mRNA; miRNA.

Conflict of interest statement

Ethics approval and consent to participate

No human subjects were involved in this study. For the procedures used and material collected, no formal ethics approval is needed. All experimental procedures and animal handling complied with the guidelines of Norwegian regulation for laboratory animal experimentation (The Norwegian Animal Protection Act, No. 73 of 20 December 1974, Section 20–22, amended 19 June 2009).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Gene Ontology (GO) classification for transcriptome from Atlantic salmon eggs. Only the top-10 significantly enriched GO-terms are presented for the three categories: biological processes, cellular components, and molecular functions. X-axis shows the number of unique genes enriched in the displayed terms. The detailed GO annotation is given in Additional file 2
Fig. 2
Fig. 2
Dynamics of postovulatory transcriptome in Atlantic salmon egg obtained from a) good and b) poor egg quality group. Transcripts with similar expression pattern were clustered and represented by the scaled mean expression value at each sampling time. The dynamics of transcripts was obtained by self-organizing map clustering of individual transcripts at three time points: at the onset of ovulation, at 14, and at the 28 days post-ovulation (0dpo, 14dpo, and 28dpo, respectively). Number of differentially accumulated transcripts between the sampling time-points is shown for 28dpo vs 0dpo (orange), 28dpo vs 14dpo (blue) and 14dpo vs 0dpo (red) comparisons. The details of discrimination between the two quality groups are given in the text (see also Additional file 3). Y-axis is scaled expression level of transcripts. n is the number of transcripts showing a given expression pattern during the postovulatory aging. Nine different patterns for each egg quality group are displayed
Fig. 3
Fig. 3
Number of significantly enriched transcripts in Atlantic salmon eggs throughout the postovulatory retention in the body cavity. Comparison of good versus poor quality egg batches (n = 6 each) in the three time points (days post-ovulation, dpo) and comparison of the time points within each egg quality group are given. Pairwise comparisons were performed for good versus poor quality eggs for each time point (0, 14 and 28 dpo), between the time points (0 dpo versus 14 dpo; 0 dpo versus 28 dpo; and 14 dpo versus 28 dpo), as well as across quality and time point groups
Fig. 4
Fig. 4
Principal Component Analysis of mRNAs in eggs of Atlantic salmon over the course of postovulatory retention period. Transcripts are projected in the 2-dimensional plane by profile of all transcripts
Fig. 5
Fig. 5
Relative abundance of 14 selected transcripts in Atlantic salmon eggs measured by RT-qPCR method. Expression level (average from n = 6 samples with standard deviation bars) relative to exogenous reference, luciferase. * Asterisks mark signficant difference at p < 0.05
Fig. 6
Fig. 6
Diffirentially abundant miRNAs in Atlantic salmon eggs throughout the postovulatory retention period. a), good egg quality group; b), poor egg quality group; c), good versus poor quality eggs at 28 days post ovulation (dpo). Normalization is described in Materials and Methods. The error bar is standard deviation. Different letters indicate significant difference at p < 0.05
Fig. 7
Fig. 7
A posteriori developmental performance of Atlantic salmon embryos obtained from good and poor egg quality groups (n = 6 for each). a) Eyed embryos; b) survival at yolk-sac resorption. RNA-seq data were obtained from three postovulatory ages (shaded). The full experimental set-up is given at Mommens et al. [10]

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