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Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus mykiss.

ABSTRACT: BACKGROUND:Maternal transcripts are accumulated in the oocyte during oogenesis to provide for protein synthesis from oocyte maturation through early embryonic development, when nuclear transcription is silenced. The maternal mRNAs have short poly(A) tails after undergoing post-transcriptional processing necessary for stabilizing them for storage. The transcripts undergo cytoplasmic polyadenylation when they are to be translated. Transcriptome analyses comparing total mRNA and elongated poly(A) mRNA content among eggs of different quality can provide insight into molecular mechanisms affecting egg developmental competence in rainbow trout. The present study used RNA-seq to compare transcriptomes of unfertilized eggs of rainbow trout females yielding different eyeing rates, following rRNA removal and poly(A) retention for construction of the libraries. RESULTS:The percentage of embryos to reach the 32-cell stage at 24?h post fertilization was significantly correlated to family eyeing rate, indicating that inviable embryos were developmentally compromised before zygotic genome activation. RNA sequencing identified 2 differentially expressed transcripts (DETs) from total mRNA sequencing comparing females with low-quality (?80% eyeing) eggs. In contrast, RNA sequencing from poly(A) captured transcripts identified 945 DETs between low- and high-quality eggs, 1012 between low- and medium-quality eggs, and only 2 between medium- and high-quality eggs. The transcripts of mitochondrial genes were enriched with polyadenylated transcript sequencing and they were significantly reduced in low-quality eggs. Similarly, mitochondrial DNA was reduced in low-quality eggs compared with medium- and high-quality eggs. The functional gene analysis classified the 945 DETs between low- and high-quality eggs into 31 functional modules, many of which were related to ribosomal and mitochondrial functions. Other modules involved transcription, translation, cell division, apoptosis, and immune responses. CONCLUSIONS:Our results indicate that differences in egg quality may be derived from differences in maternal nuclear transcript activation and cytoplasmic polyadenylation before ovulation, as opposed to accumulation and storage of maternal nuclear transcripts during oogenesis. Transcriptome comparisons suggest low-quality eggs suffered from impaired oxidative phosphorylation and translation. The DETs identified in this study provide insight into developmental competence in rainbow trout eggs.

SUBMITTER: Ma H

PROVIDER: S-EPMC6486991 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus mykiss.

Ma Hao H Martin Kyle K Dixon Doug D Hernandez Alvaro G AG Weber Gregory M GM

BMC genomics 20190427 1

<h4>Background</h4>Maternal transcripts are accumulated in the oocyte during oogenesis to provide for protein synthesis from oocyte maturation through early embryonic development, when nuclear transcription is silenced. The maternal mRNAs have short poly(A) tails after undergoing post-transcriptional processing necessary for stabilizing them for storage. The transcripts undergo cytoplasmic polyadenylation when they are to be translated. Transcriptome analyses comparing total mRNA and elongated p ...[more]

PMID: 31029084

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Project description:BackgroundTranscription is arrested in the late stage oocyte and therefore the maternal transcriptome stored in the oocyte provides nearly all the mRNA required for oocyte maturation, fertilization, and early cleavage of the embryo. The transcriptome of the unfertilized egg, therefore, has potential to provide markers for predictors of egg quality and diagnosing problems with embryo production encountered by fish hatcheries. Although levels of specific transcripts have been shown to associate with measures of egg quality, these differentially expressed genes (DEGs) have not been consistent among studies. The present study compares differences in select transcripts among unfertilized rainbow trout eggs of different quality based on eyeing rate, among 2 year classes of the same line (A1, A2) and a population from a different hatchery (B). The study compared 65 transcripts previously reported to be differentially expressed with egg quality in rainbow trout.ResultsThere were 32 transcripts identified as DEGs among the three groups by regression analysis. Group A1 had the most DEGs, 26; A2 had 15, 14 of which were shared with A1; and B had 12, 7 of which overlapped with A1 or A2. Six transcripts were found in all three groups, dcaf11, impa2, mrpl39_like, senp7, tfip11 and uchl1.ConclusionsOur results confirmed maternal transcripts found to be differentially expressed between low- and high-quality eggs in one population of rainbow trout can often be found to overlap with DEGs in other populations. The transcripts differentially expressed with egg quality remain consistent among year classes of the same line. Greater similarity in dysregulated transcripts within year classes of the same line than among lines suggests patterns of transcriptome dysregulation may provide insight into causes of decreased viability within a hatchery population. Although many DEGs were identified, for each of the genes there is considerable variability in transcript abundance among eggs of similar quality and low correlations between transcript abundance and eyeing rate, making it highly improbable to predict the quality of a single batch of eggs based on transcript abundance of just a few genes.

Project description:BackgroundGenetic maps characterizing the inheritance patterns of traits and markers have been developed for a wide range of species and used to study questions in biomedicine, agriculture, ecology and evolutionary biology. The status of rainbow trout genetic maps has progressed significantly over the last decade due to interest in this species in aquaculture and sport fisheries, and as a model research organism for studies related to carcinogenesis, toxicology, comparative immunology, disease ecology, physiology and nutrition. We constructed a second generation genetic map for rainbow trout using microsatellite markers to facilitate the identification of quantitative trait loci for traits affecting aquaculture production efficiency and the extraction of comparative information from the genome sequences of model fish species.ResultsA genetic map ordering 1124 microsatellite loci spanning a sex-averaged distance of 2927.10 cM (Kosambi) and having 2.6 cM resolution was constructed by genotyping 10 parents and 150 offspring from the National Center for Cool and Cold Water Aquaculture (NCCCWA) reference family mapping panel. Microsatellite markers, representing pairs of loci resulting from an evolutionarily recent whole genome duplication event, identified 180 duplicated regions within the rainbow trout genome. Microsatellites associated with genes through expressed sequence tags or bacterial artificial chromosomes produced comparative assignments with tetraodon, zebrafish, fugu, and medaka resulting in assignments of homology for 199 loci.ConclusionThe second generation NCCCWA genetic map provides an increased microsatellite marker density and quantifies differences in recombination rate between the sexes in outbred populations. It has the potential to integrate with cytogenetic and other physical maps, identifying paralogous regions of the rainbow trout genome arising from the evolutionarily recent genome duplication event, and anchoring a comparative map with the zebrafish, medaka, tetraodon, and fugu genomes. This resource will facilitate the identification of genes affecting traits of interest through fine mapping and positional cloning of candidate genes.

Dataset Information

Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus mykiss.

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Transcriptome analysis of egg viability in rainbow trout, Oncorhynchus mykiss.

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