Abstract

Maternal mRNA present in mature oocytes plays an important role in the proper development of the early embryo. As the composition of the maternal transcriptome in general has been studied with pooled mature eggs, potential differences between individual eggs are unknown. Here we present a transcriptome study on individual zebrafish eggs from clutches of five mothers in which we focus on the differences in maternal mRNA abundance per gene between and within clutches. To minimize technical interference, we used mature, unfertilized eggs from siblings. About half of the number of analyzed genes was found to be expressed as maternal RNA. The expressed and non-expressed genes showed that maternal mRNA accumulation is a non-random process, as it is related to specific biological pathways and processes relevant in early embryogenesis. Moreover, it turned out that overall the composition of the maternal transcriptome is tightly regulated as about half of the expressed genes display a less than twofold expression range between the observed minimum and maximum expression values of a gene in the experiment. Even more, the maximum gene-expression difference within clutches is for 88% of the expressed genes lower than twofold. This means that expression differences observed in maternally expressed genes are primarily caused by differences between mothers, with only limited variability between eggs from the same mother. This was underlined by the fact that 99% of the expressed genes were found to be differentially expressed between any of the mothers in an ANOVA test. Furthermore, linking chromosome location, transcription factor binding sites, and miRNA target sites of the genes in clusters of distinct and unique mother-specific gene-expression, suggest biological relevance of the mother-specific signatures in the maternal transcriptome composition. Altogether, the maternal transcriptome composition of mature zebrafish oocytes seems to be tightly regulated with a distinct mother-specific signature.

Highlights

  • Maternal RNA is defined as those transcripts present in a mature oocyte orfertilized egg before the initiation of zygotic gene expression [1,2]

  • Little is known about the differences in the maternal transcriptomes between individual Zebrafish eggs, as to our knowledge in all published studies on transcriptome dynamics in early embryogenesis eggs are pooled for analysis [16,17,18,19,48]

  • To get a first impression of the variability of the maternal transcriptome between individual eggs, we examined per gene the maximum fold change, i.e. the highest measured intensity divided by the lowest

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Summary

Introduction

Maternal RNA is defined as those transcripts present in a mature oocyte or (un)fertilized egg before the initiation of zygotic gene expression [1,2]. Their significance is reflected in the enormous amounts, up to several ug total RNA per egg in oviparous species [3]. But still in the Prophase I of the meiosis chromosomes unpair and the developing oocyte starts a long period of cytoplasmic growth In this lengthy developmental phase the maternal RNA molecules are either produced by the oocyte or deposited by surrounding cells into the oocyte during oogenesis [5,6]. Fish maternal mRNA is intensively studied because zebrafish (Danio rerio) is an increasingly popular model organism [14] and maternal RNAs are considered important determinants of egg quality in farmed fish [15]

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