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Egg transcriptome reveals molecular signature to predict developmental success and novel maternal-effect genes

ABSTRACT: Good quality or developmentally competent eggs result in high survival of progeny. Previous research has shed light on factors that determine egg quality, however, large gaps remain. Initial development of the embryo relies on maternally-inherited molecules, such as transcripts, deposited in the egg, thus, they would likely reflect egg quality. We performed microarray analysis on zebrafish fertilized eggs of different quality from unrelated, wildtype couples to obtain a global portrait of the egg transcriptome to determine its association with developmental competence and to identify new candidate maternal-effect genes. Fifteen of the most differentially expressed genes (DEGs) were validated by quantitative real-time PCR. Gene ontology analysis showed that enriched terms included ribosomes and translation. In addition, statistical modeling using partial least squares regression and genetics algorithm also demonstrated that gene signatures from the transcriptomic data can be used to predict reproductive success. Among the validated DEGs, otulina and slc29a1a were found to be increased in good quality eggs and to be predominantly localized in the ovaries. CRISPR/Cas9 knockout mutants of each gene revealed remarkable subfertility whereby the majority of their embryos were unfertilizable.Our novel findings suggested that even in varying quality of eggs due to heterogeneous causes from unrelated wildtype couples, gene signatures exist in the egg transcriptome, which can be used to predict developmental competence. Further, transcriptomic profiling revealed two new potential maternal-effect genes that have essential roles in vertebrate reproduction.

ORGANISM(S): Danio rerio

PROVIDER: GSE109073 | GEO | 2019/02/01

REPOSITORIES: GEO

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Project description:Molecular profiling of the eggs is an excellent approach aiming at understanding biological processes and mechanisms conditioning developmental competence in finfishes and, consequently, reproductive fitness. Despite many efforts, it is still unclear what is the specific role of transcriptome and proteome in determination of egg quality in Teleostei fishes. The aim of this study was to perform integrated transcriptomic-proteomic analysis of eggs of pikeperch – a commercially relevant freshwater fish species. Additionally, comparative analysis of transcriptome and proteome in eggs characterized by either high or low egg quality has been performed, in order to identify mechanisms leading to early embryonic lethality in pikeperch. Our study provides a novel insight into the understanding of the role of maternally-derived molecular cargo in finfishes. The data obtained sheds light on the importance of transcriptome in development of nervous system suggesting neurogenesis-related mRNAs as a very important, non-genetic inheritance factor. Proteomic analysis highlights specific role of proteins in the immune response in ovulated eggs. Integrated analysis brings attention to the galactose-specific lectin nattectin gene and protein as the frontline defense molecule for the egg and developing embryo. The molecular analysis of egg developmental competence emphasizes post-vitellogenic processes (final oocyte maturation and ovulation) as the ones potentially compromising transcriptomic profile, but not affecting proteomic cargo. It highlights the need for careful reconsideration of the commercial reproductive protocols as the very strong modulators of egg quality and their molecular profile. Considering the mechanisms driving these alterations as well as consequences stemming from the differential abundance of the transcripts are still to be explored, the candidate quality markers, first time provided for pikeperch along with the current study, are creating valuable resource for further studies.

Project description:Gynogenetic development in fish is induced by activation of eggs with irradiated spermatozoa followed by exposure of the activated eggs to the temperature or high hydrostatic pressure (HHP) shock that prevents 1st cell cleavage. Produced specimens are fully homozygous fish also known as Doubled Haploids. Gynogenetic DH individuals might be used aquaculture and developmental biology unfortunately; the potential application of DHs is limited by a rather low survival rate of such specimens. However, observed variation in the survival rates of the gynogenetic embryos originated from different clutches suggests that eggs from some females have increased ability for gynogenetic development than others. Taking into account that first 10 cell cleavages in the fish embryos rely on the maternal RNA, it is tempting to assume that the ova showing such a vast difference in potential for gynogenesis may have also had different biological characteristics including alterations in maternal gene expression profiles. If so, then genes that up- or down –regulated expression in eggs increases competence for gynogenetic development in trout might be considered as candidate genes for gynogenesis in rainbow trout. Thus, the main goal of the project is identification of genes that increase ability of rainbow trout eggs for gynogenetic development. Within the project, we tried to verify following hypotheses: 1. Eggs from different females have different potential for gynogenesis in rainbow trout. 2. Eggs with different ability for gynogenetic development with all maternal inheritance have different biological characteristics including morphology and anti-ROS enzyme activities. 3. Eggs with increased competence for gynogenesis have altered transcriptomic profiles. 4. There are some particular genes that altered expression in trout eggs enable development of gynogenetic embryos. Gynogenetic rainbow trout specimens were produced in the course of activation of eggs with UV-irradiated spermatozoa and High Hydrostatic Pressure shock (HHP) applied around 1st cell cleavage. Eggs from several females were used in the experiment. Survival rates of gynogenetic rainbow trout was monitored since fertilization. Quality of eggs was examined by assessment of their morphology and activity of anti-ROS (reactive oxygene species) enzymes. Transcriptome of eggs showing increased and decreased developmental competence for gynogenesis was analyzed using RNA-seq approach and results compared to find out any alterations related to survival of gynogenetic trout.

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Egg transcriptome reveals molecular signature to predict developmental success and novel maternal-effect genes

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