Abstract
BackgroundThe development of multicellular organisms is accompanied by gene expression changes in differentiating cells. Profiling stage-specific expression during development may reveal important insights into gene sets that contributed to the morphological diversity across the animal kingdom.ResultsWe sequenced RNA-seq libraries throughout a developmental timecourse of the nematode Pristionchus pacificus. The transcriptomes reflect early larval stages, adult worms including late larvae, and growth-arrested dauer larvae and allowed the identification of developmentally regulated gene clusters. Our data reveals similar trends as previous transcriptome profiling of dauer worms and represents the first expression data for early larvae in P. pacificus. Gene expression clusters characterizing early larval stages show most significant enrichments of chaperones, while collagens are most significantly enriched in transcriptomes of late larvae and adult worms. By combining expression data with phylogenetic analysis, we found that developmentally regulated genes are found in paralogous clusters that have arisen through lineage-specific duplications after the split from the Caenorhabditis elegans branch.ConclusionsWe propose that gene duplications of developmentally regulated genes represent a plausible evolutionary mechanism to increase the dosage of stage-specific expression. Consequently, this may contribute to the substantial divergence in expression profiles that has been observed across larger evolutionary time scales.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0466-2) contains supplementary material, which is available to authorized users.
Highlights
The development of multicellular organisms is accompanied by gene expression changes in differentiating cells
We identify and characterize gene clusters with developmentalstage specific expression and use phylogenetic analyses to test for conservation of stage-specific expressed genes
We evaluated the quality of one-to-one orthology predictions using a data set of 107 C. elegans genes for which orthology relationships were manually investigated using alternative versions of P. pacificus gene predictions, TBLASTN searches to complement incomplete gene models, and subsequent phylogenetic analysis including all potential paralogous sequences
Summary
The development of multicellular organisms is accompanied by gene expression changes in differentiating cells. The development from a single cell progenitor to a fully grown multicellular organism with up to hundreds of tissue types is accompanied by differentiation processes that change the transcriptional state, i.e. the levels of gene expression within each cell type. The nematode Caenorhabditis elegans has been proven as a highly attractive model for studying developmental biology, as its ontogenesis resembles an almost completely deterministic process that results in a fixed number of cells in the mature animal. For C. elegans and P. pacificus, the same features that make them excellent model organisms for studying the genetics of developmental processes, such as their small size and short generation time, complicate detailed studies of development on a transcriptional level. Sinha et al showed that, despite the fact that some key actors initiating the signaling cascades into dauer entry are conserved between C. elegans and P. pacificus [4], dauer specific transcriptome profiles show substantial divergence with only 184 genes that showed dauerspecific differential regulation in both species, of which 68 genes even exhibited opposing trends with respect to up and downregulation [9]
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