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Comparative Study
, 58 (6-8), 501-11

A Conserved Set of Maternal Genes? Insights From a Molluscan Transcriptome

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Comparative Study

A Conserved Set of Maternal Genes? Insights From a Molluscan Transcriptome

M Maureen Liu et al. Int J Dev Biol.

Abstract

The early animal embryo is entirely reliant on maternal gene products for a 'jump-start' that transforms a transcriptionally inactive embryo into a fully functioning zygote. Despite extensive work on model species, it has not been possible to perform a comprehensive comparison of maternally-provisioned transcripts across the Bilateria because of the absence of a suitable dataset from the Lophotrochozoa. As part of an ongoing effort to identify the maternal gene that determines left-right asymmetry in snails, we have generated transcriptome data from 1 to 2-cell and ~32-cell pond snail (Lymnaea stagnalis) embryos. Here, we compare these data to maternal transcript datasets from other bilaterian metazoan groups, including representatives of the Ecydysozoa and Deuterostomia. We found that between 5 and 10% of all L. stagnalis maternal transcripts (~300-400 genes) are also present in the equivalent arthropod (Drosophila melanogaster), nematode (Caenorhabditis elegans), urochordate (Ciona intestinalis) and chordate (Homo sapiens, Mus musculus, Danio rerio) datasets. While the majority of these conserved maternal transcripts ("COMATs") have housekeeping gene functions, they are a non-random subset of all housekeeping genes, with an overrepresentation of functions associated with nucleotide binding, protein degradation and activities associated with the cell cycle. We conclude that a conserved set of maternal transcripts and their associated functions may be a necessary starting point of early development in the Bilateria. For the wider community interested in discovering conservation of gene expression in early bilaterian development, the list of putative COMATs may be useful resource.

Figures

Fig. 1
Fig. 1. Enrichment of Gene Ontology terms in the conserved maternal transcript (COMAT) subset
Highest level GO terms that show the greatest enrichment in COMAT compared with the L. stagnalis 1 to 2-cell transcriptome. Only those comparisons with P < 1E-5 are shown. Black shading: percentage of each type in COMAT. Grey shading: percentage of each type in the 1 to 2-cell transcriptome.
Fig. 2
Fig. 2. Visualisation of maternal gene product spatial distribution in uncleaved zygotes of Lymnaea stagnalis by whole mount in situ hybridisation
Eight maternal gene products were visualised in uncleaved zygotes relative to a negative control (β-tubulin). (A) β-tubulin is not detectable in uncleaved zygotes. A polar body is indicated by the horizontal arrow. (B) β-tubulin is clearly expressed in ciliated cells of older veliger larvae. (C) contig_2724: ATP-dependent RNA helicase dhx8. (D) contig_453: heat shock 70 kda protein cognate 4. (E) contig_7974: ADP-ribosylation factor 4. (F) contig_9053: proteasome alpha 6 subunit. (G) contig_579: ergic and golgi 2. (H) contig_9016: eukaryotic translation initiation factor 3 subunit i. (I) contig_8075: eukaryotic translation elongation factor. (J) contig_8318: 78 kda glucose-regulated protein.
Fig. 3
Fig. 3. Frequency histogram of relative gene expression for human housekeeping genes
Conserved maternal transcripts (COMATs, red line) tend to have a higher gene expression (measured reads per kb per million mapped reads, RPKM) than non-COMATs (blue). However, COMATs still represent several orders of magnitude of gene expression. Gene expression data from Eisenberg & Levanon (2013).

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