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Comparative transcriptomics reveal developmental turning points during embryogenesis of a hemimetabolous insect, the damselfly Ischnura elegans.

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.

SUBMITTER: Simon S

PROVIDER: S-EPMC5648782 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Comparative transcriptomics reveal developmental turning points during embryogenesis of a hemimetabolous insect, the damselfly Ischnura elegans.

Simon Sabrina S Sagasser Sven S Saccenti Edoardo E Brugler Mercer R MR Schranz M Eric ME Hadrys Heike H Amato George G DeSalle Rob R

Scientific reports 20171019 1

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 ...[more]

PMID: 29051502

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Project description:BackgroundUnderstanding and predicting how organisms respond to human-caused environmental changes has become a major concern in conservation biology. Here, we linked gene expression and phenotypic data to identify candidate genes underlying existing phenotypic trait differentiation under individual and combined environmental variables. For this purpose, we used the damselfly Ischnura elegans. Egg clutches from replicated high- (southern Sweden) and central-latitude (southern Poland) populations facing different degrees of seasonal time constraints were collected. Damselfly larvae were exposed to experimental treatments: current and mild warming temperatures crossed with the presence or absence of an invasive alien predator cue released by the spiny-cheek crayfish, Faxonius limosus, which is only present in Poland to date. We measured the following traits: larval development time, body size, mass and growth rate, and used the larvae for gene expression analysis by RNA-seq. Data were analysed using a multivariate approach.ResultsWe showed latitudinal differences in coping with mild warming and predator cues. When exposed to an increased temperature and a predator cue, central-latitude individuals had the shortest development and the fastest growth compared to high-latitude individuals. There was a general effect of predator cues regarding mass and growth rate reduction independent of latitude. Transcriptome analysis revealed that metabolic pathways related to larval anatomy and development tended to be upregulated in response to mild warming but only in fast-growing central-latitude individuals. Metabolic pathways linked to oxidative stress tended to be downregulated in response to a predator cue, especially in central-latitude individuals.ConclusionDifferent phenotypic and transcriptomic responses to environmental factors might be attributed to the variability in I. elegans life history strategies between the two latitudes caused by seasonal time constraints and to its coexistence with the invasive alien predator in nature. By providing insights into how organisms may respond to future anthropogenic changes, our results may be of particular interest in conservation biology.

Dataset Information

Comparative transcriptomics reveal developmental turning points during embryogenesis of a hemimetabolous insect, the damselfly Ischnura elegans.

Publications

Comparative transcriptomics reveal developmental turning points during embryogenesis of a hemimetabolous insect, the damselfly Ischnura elegans.

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