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Proceedings of the National Academy of Sciences
Article . 2023 . Peer-reviewed
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Reduction of embryonicE93expression as a hypothetical driver of the evolution of insect metamorphosis

Authors: Ana Fernandez-Nicolas; Gabriela Machaj; Alba Ventos-Alfonso; Viviana Pagone; Toshinori Minemura; Takahiro Ohde; Takaaki Daimon; +2 Authors

Reduction of embryonicE93expression as a hypothetical driver of the evolution of insect metamorphosis

Abstract

The early embryo of the cockroachBlattella germanicaexhibits highE93expression. In general, E93 triggers adult morphogenesis during postembryonic development. Here we show that E93 is also crucial in early embryogenesis in the cockroach, as a significant number of E93-depleted embryos are unable to develop the germ band under maternal RNAi treatment targetingE93. Moreover, transcriptomic analysis indicates that E93 depletion results in important gene expression changes in the early embryo, and many of the differentially expressed genes are involved in development. Then, using public databases, we gatheredE93expression data in embryo and preadult stages, finding that embryonic expression ofE93is high in hemimetabolan species (whose juveniles, or nymphs, are similar to the adult) and low in holometabolans (whose juveniles, or larvae, are different from the adult).E93expression is also low in Thysanoptera and in Hemiptera Sternorrhyncha, hemimetabolans with postembryonic quiescent stages, as well as in Odonata, the nymph of which is very different from the adult. In ametabolans, such as the ZygentomaThermobia domestica,E93transcript levels are very high in the early embryo, whereas during postembryonic development they are medium and relatively constant. We propose the hypothesis that during evolution, a reduction ofE93expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases ofE93transcripts in the embryo of Odonata, Thysanoptera, and different groups of Hemiptera Sternorrhyncha would have allowed the development of modified juvenile stages adapted to specific ecophysiological conditions.

Countries
Poland, Spain
Keywords

Insecta, Insect metamorphosis, complex life cycles, Metamorphosis, Biological, Gene Expression Regulation, Developmental, Complex life cycles, Biological Sciences, Hemiptera, E93, Larva, Embryogenesis, Animals, Insect Proteins, insect metamorphosis, embryogenesis, RNA Interference

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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
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