Abstract
Identifying transcriptional changes during embryogenesis is of crucial importance for unravelling evolutionary, molecular and cellular mechanisms that underpin patterning and morphogenesis. However, comparative studies focusing on early/embryonic stages during insect development are limited to a few taxa. Drosophila melanogaster is the paradigm for insect development, whereas comparative transcriptomic studies of embryonic stages of hemimetabolous insects are completely lacking. We reconstructed the first comparative transcriptome covering the daily embryonic developmental progression of the blue-tailed damselfly Ischnura elegans (Odonata), an ancient hemimetabolous representative. We identified a “core” set of 6,794 transcripts – shared by all embryonic stages – which are mainly involved in anatomical structure development and cellular nitrogen compound metabolic processes. We further used weighted gene co-expression network analysis to identify transcriptional changes during Odonata embryogenesis. Based on these analyses distinct clusters of transcriptional active sequences could be revealed, indicating that embryos at different development stages have their own transcriptomic profile according to the developmental events and leading to sequential reprogramming of metabolic and developmental genes. Interestingly, a major change in transcriptionally active sequences is correlated with katatrepsis (revolution) during mid-embryogenesis, a 180° rotation of the embryo within the egg and specific to hemimetabolous insects.
Highlights
During embryogenesis, the central life cycle, the embryonic body plan is laid out, starting with blastoderm formation, germ band formation, followed by elongation, segmentation, and appendage formation
We present the first comprehensive embryonic transcriptome of a hemimetabolous insect, the damselfly I. elegans
Using a single-embryo sequencing approach we were able to elucidate the transcriptional divergence of pre- and post-revolutionary embryonic stages highlighting the transcriptional complexity during insect embryogenesis
Summary
The central life cycle, the embryonic body plan is laid out, starting with blastoderm formation, germ band formation, followed by elongation, segmentation, and appendage formation. The involvement of genes in specific developmental processes is usually determined on a small scale by comparing expression patterns of specific key genes across species by means of in situ hybridization or quantitative RT-PCR. We generated expression data throughout all embryonic developmental stages covering germ band formation, elongation, segmentation, and appendage formation, by performing comprehensive RNA sequencing on single I. elegans embryos. Based on this RNA-seq data we developed a novel I. elegans reference transcriptome and examined gene expression divergence across all embryonic stages to provide novel insights in the genetics of embryogenesis of a hemimetabolous insect. Our comparative data will provide insights into the extent of gene expression variation during embryogenesis in more “primitive” hemimetabolous lineages
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