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What makes a bad egg? Egg transcriptome reveals dysregulation of translational machinery and novel fertility genes important for fertilization

  • Cheung, Caroline
  • Nguyen, Thuy Thao Vi
  • Le Cam, Aurélie
  • Patinote, Amélie
  • Journot, Laurent
  • Reynes, Christelle
  • Bobe, Julien
Publication Date
Jan 01, 2019
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Background: Egg quality can be defined as the egg ability to be fertilized and subsequently develop into a normalembryo. Previous research has shed light on factors that can influence egg quality. Large gaps however remainincluding a comprehensive view of what makes a bad egg. Initial development of the embryo relies on maternallyinherited molecules, such as transcripts, deposited in the egg during its formation. Bad egg quality is thereforesusceptible to be associated with alteration or dysregulation of maternally-inherited transcripts. We performedtranscriptome analysis on a large number (N = 136) of zebrafish egg clutches, each clutch being split to monitordevelopmental success and perform transcriptome analysis in parallel. We aimed at drawing a molecular portrait ofthe egg in order to characterize the relation between egg transcriptome and developmental success and tosubsequently identify new candidate genes involved in fertility.Results: We identified 66 transcript that were differentially abundant in eggs of contrasted phenotype (low or highdevelopmental success). Statistical modeling using partial least squares regression and genetics algorithmdemonstrated that gene signatures from transcriptomic data can be used to predict developmental success. Theidentity and function of differentially expressed genes indicate a major dysregulation of genes of the translationalmachinery in poor quality eggs. Two genes, otulina and slc29a1a, predominantly expressed in the ovary anddysregulated in poor quality eggs were further investigated using CRISPR/Cas9 mediated genome editing. Mutantsof each gene revealed remarkable subfertility whereby the majority of their eggs were unfertilizable. The Wntpathway appeared to be dysregulated in the otulina mutant-derived eggs.Conclusions: Here we show that egg transcriptome contains molecular signatures, which can be used to predictdevelopmental success. Our results also indicate that poor egg quality in zebrafish is associated with adysregulation of (i) the translational machinery genes and (ii) novel fertility genes, otulina and slc29a1a, playing animportant role for fertilization. Together, our observations highlight the diversity of the possible causes of eggquality defects and reveal mechanisms of maternal origin behind the lack of fertilization and early embryonicfailures that can occur under normal reproduction conditions.

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