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

Autor: Christelle Reynes, Thuy Thao Vi Nguyen, Caroline Cheung, Aurélie Le Cam, Julien Bobe, Amélie Patinote, Laurent Journot
Přispěvatelé: Laboratoire de Physiologie et Génomique des Poissons (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Institut National de la Recherche Agronomique (INRA), Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX), Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), ANR-13-BSV7–0015-Maternal Legacy, ANR-13-BSV7-0015-Maternal Legacy, Agence Nationale de la Recherche, ANR-13-BSV7-0015,Maternal Legacy,Portait moléculaire d'un oeuf de poisson de bonne qualité(2013)
Rok vydání: 2019
Předmět:
0106 biological sciences
Male
Candidate gene
[SDV]Life Sciences [q-bio]
poisson zèbre
Microarray
01 natural sciences
Transcriptome
oeuf de poisson
Human fertilization
poisson
cyprinidae
ontology
Zebrafish
Wnt Signaling Pathway
développement de l'embryon
ontologie
Genetics
0303 health sciences
fécondation
egg quality
transcriptome
microarray
zebrafish
differentially expressed genes
prediction model
Embryo
transcrit
Phenotype
danio rerio
embryonic structures
Female
DNA microarray
transcription
danio devario
Egg quality
Biotechnology
expression des gènes
Research Article
lcsh:QH426-470
qualité des oeufs
lcsh:Biotechnology
bacterialresistance transfer factor
Biology
Real-Time Polymerase Chain Reaction
reproduction
fertilité
03 medical and health sciences
Prediction model
lcsh:TP248.13-248.65
Animals
Gene
CRISPR/Cas9
030304 developmental biology
Ovum
fish
biology.organism_classification
modèle prédictif
sex factors
lcsh:Genetics
Fertility
Gene Expression Regulation
Protein Biosynthesis
Differentially expressed genes
010606 plant biology & botany
Zdroj: BMC Genomics
BMC Genomics (20:584), 1-14. (2019)
BMC Genomics, BioMed Central, 2019, 20:584 (1), pp.1-14. ⟨10.1186/s12864-019-5930-8⟩
BMC Genomics, Vol 20, Iss 1, Pp 1-14 (2019)
ISSN: 1471-2164
DOI: 10.1186/s12864-019-5930-8⟩
Popis: Background Egg quality can be defined as the egg ability to be fertilized and subsequently develop into a normal embryo. Previous research has shed light on factors that can influence egg quality. Large gaps however remain including a comprehensive view of what makes a bad egg. Initial development of the embryo relies on maternally-inherited molecules, such as transcripts, deposited in the egg during its formation. Bad egg quality is therefore susceptible to be associated with alteration or dysregulation of maternally-inherited transcripts. We performed transcriptome analysis on a large number (N = 136) of zebrafish egg clutches, each clutch being split to monitor developmental success and perform transcriptome analysis in parallel. We aimed at drawing a molecular portrait of the egg in order to characterize the relation between egg transcriptome and developmental success and to subsequently identify new candidate genes involved in fertility. Results We identified 66 transcript that were differentially abundant in eggs of contrasted phenotype (low or high developmental success). Statistical modeling using partial least squares regression and genetics algorithm demonstrated that gene signatures from transcriptomic data can be used to predict developmental success. The identity and function of differentially expressed genes indicate a major dysregulation of genes of the translational machinery in poor quality eggs. Two genes, otulina and slc29a1a, predominantly expressed in the ovary and dysregulated in poor quality eggs were further investigated using CRISPR/Cas9 mediated genome editing. Mutants of each gene revealed remarkable subfertility whereby the majority of their eggs were unfertilizable. The Wnt pathway 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 predict developmental success. Our results also indicate that poor egg quality in zebrafish is associated with a dysregulation of (i) the translational machinery genes and (ii) novel fertility genes, otulina and slc29a1a, playing an important role for fertilization. Together, our observations highlight the diversity of the possible causes of egg quality defects and reveal mechanisms of maternal origin behind the lack of fertilization and early embryonic failures that can occur under normal reproduction conditions. Electronic supplementary material The online version of this article (10.1186/s12864-019-5930-8) contains supplementary material, which is available to authorized users.
Databáze: OpenAIRE
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