title: Maternally inherited npm2 mRNA is crucial for egg developmental competence in zebrafish.
abstract: The molecular mechanisms underlying and determining egg developmental competence remain poorly understood in vertebrates. Nucleoplasmin (Npm2) is one of the few known maternal effect genes in mammals, but this maternal effect has never been demonstrated in nonmammalian species. A link between developmental competence and the abundance of npm2 maternal mRNA in the egg was previously established using a teleost fish model for egg quality. The importance of maternal npm2 mRNA for egg developmental competence remains unknown in any vertebrate species. In the present study, we aimed to characterize the contribution of npm2 maternal mRNA to early developmental success in zebrafish using a knockdown strategy. We report here the oocyte-specific expression of npm2 and maternal inheritance of npm2 mRNA in zebrafish eggs. The knockdown of the protein translated from this maternal mRNA results in developmental arrest before the onset of epiboly and subsequent embryonic death, a phenotype also observed in embryos lacking zygotic transcription. Npm2 knockdown also results in impaired transcription of the first-wave zygotic genes. Our results show that npm2 is also a maternal effect gene in a nonmammalian vertebrate species and that maternally inherited npm2 mRNA is crucial for egg developmental competence. We also show that de novo protein synthesis from npm2 maternal mRNA is critical for developmental success beyond the blastula stage and required for zygotic genome activation. Finally, our results suggest that npm2 maternal mRNA is an important molecular factor of egg quality in fish and possibly in all vertebrates.
authors.affiliation: INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France IFREMER, LALR, Palavas-Les-Flots, France.
authors.forename: Aurélien
authors.initials: A
authors.lastname: Bouleau
authors.affiliation: INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France IFREMER, LALR, Palavas-Les-Flots, France.
authors.forename: Thomas
authors.initials: T
authors.lastname: Desvignes
authors.affiliation: INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France.
authors.forename: Juan Martin
authors.initials: JM
authors.lastname: Traverso
authors.affiliation: INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France.
authors.forename: Thaovi
authors.initials: T
authors.lastname: Nguyen
authors.affiliation: CNRS/UMR6290, University of Rennes 1, Rennes, France.
authors.forename: Franck
authors.initials: F
authors.lastname: Chesnel
authors.affiliation: IFREMER, LALR, Palavas-Les-Flots, France.
authors.forename: Christian
authors.initials: C
authors.lastname: Fauvel
authors.affiliation: INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France julien.bobe@rennes.inra.fr.
authors.forename: Julien
authors.initials: J
authors.lastname: Bobe
mesh_terms: D000818:Animals; D004625:Embryo, Nonmammalian; D005260:Female; D005786:Gene Expression Regulation / Q000502:physiology; D055785:Gene Knockdown Techniques; D060172:Morpholinos; D056489:Nucleoplasmins / Q000235:genetics / Q000378:metabolism*; D010063:Ovum / Q000166:cytology* / Q000502:physiology*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D059467:Transcriptome; D015027:Zebrafish / Q000235:genetics / Q000378:metabolism*; D029961:Zebrafish Proteins / Q000235:genetics / Q000378:metabolism*
chemical_list: D060172:Morpholinos; D056489:Nucleoplasmins; D012333:RNA, Messenger; D029961:Zebrafish Proteins; C000597006:npm2b protein, zebrafish
keywords: egg quality; fish; maternal effect gene; maternal-to-zygotic transition; nucleoplasmin; oocyte developmental competence; teleost; zygotic genome activation