Convergent evolution of venom gland transcriptomes across Metazoa
| Autor: | Marc Robinson-Rechavi, Giulia Zancolli, Maarten J.M.F. Reijnders, Robert M. Waterhouse |
|---|---|
| Jazyk: | angličtina |
| Rok vydání: | 2022 |
| Předmět: |
Evolution
venom Animal Structures/metabolism Animals Evolution Molecular Phylogeny Transcriptome Venoms/biosynthesis Venoms/genetics convergent evolution evolutionary novelties gene expression stress response Venom Biology 03 medical and health sciences 0302 clinical medicine Phylogenetics Convergent evolution Gene expression Secretion 030304 developmental biology 0303 health sciences Multidisciplinary Venoms Animal Structures Biological Sciences Evolutionary biology Unfolded protein response Function (biology) 030217 neurology & neurosurgery |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 1, pp. e2111392119 Proceedings of the National Academy of Sciences of the United States of America |
| Popis: | Significance On more than 100 occasions, animals have independently evolved the ability to produce and deliver potent secretions to subdue prey or predators—venom. This prompts the following question: Have animals repeatedly adopted the same genetic toolkit for venom production? In this study, we found, surprisingly, that the venom glands of different animal lineages had similar global gene expression patterns. Notably, groups of genes involved in protein secretion, and especially stress response pathways, had similar expression levels, revealing that many animals have come up with the same solution independently. On the other hand, signaling and regulatory networks had lineage-specific patterns, suggesting that the way in which cells are regulated and communicate might reflect the diverse developmental origins of venom systems. Animals have repeatedly evolved specialized organs and anatomical structures to produce and deliver a mixture of potent bioactive molecules to subdue prey or predators—venom. This makes it one of the most widespread, convergent functions in the animal kingdom. Whether animals have adopted the same genetic toolkit to evolved venom systems is a fascinating question that still eludes us. Here, we performed a comparative analysis of venom gland transcriptomes from 20 venomous species spanning the main Metazoan lineages to test whether different animals have independently adopted similar molecular mechanisms to perform the same function. We found a strong convergence in gene expression profiles, with venom glands being more similar to each other than to any other tissue from the same species, and their differences closely mirroring the species phylogeny. Although venom glands secrete some of the fastest evolving molecules (toxins), their gene expression does not evolve faster than evolutionarily older tissues. We found 15 venom gland–specific gene modules enriched in endoplasmic reticulum stress and unfolded protein response pathways, indicating that animals have independently adopted stress response mechanisms to cope with mass production of toxins. This, in turn, activates regulatory networks for epithelial development, cell turnover, and maintenance, which seem composed of both convergent and lineage-specific factors, possibly reflecting the different developmental origins of venom glands. This study represents a first step toward an understanding of the molecular mechanisms underlying the repeated evolution of one of the most successful adaptive traits in the animal kingdom. |
| Databáze: | OpenAIRE |
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