Abstract
BackgroundMost of the known genes required for developmental processes have been identified by genetic screens in a few well-studied model organisms, which have been considered representative of related species, and informative—to some degree—for human biology. The fruit fly Drosophila melanogaster is a prime model for insect genetics, and while conservation of many gene functions has been observed among bilaterian animals, a plethora of data show evolutionary divergence of gene function among more closely-related groups, such as within the insects. A quantification of conservation versus divergence of gene functions has been missing, without which it is unclear how representative data from model systems actually are.ResultsHere, we systematically compare the gene sets required for a number of homologous but divergent developmental processes between fly and beetle in order to quantify the difference of the gene sets. To that end, we expanded our RNAi screen in the red flour beetle Tribolium castaneum to cover more than half of the protein-coding genes. Then we compared the gene sets required for four different developmental processes between beetle and fly. We found that around 50% of the gene functions were identified in the screens of both species while for the rest, phenotypes were revealed only in fly (~ 10%) or beetle (~ 40%) reflecting both technical and biological differences. Accordingly, we were able to annotate novel developmental GO terms for 96 genes studied in this work. With this work, we publish the final dataset for the pupal injection screen of the iBeetle screen reaching a coverage of 87% (13,020 genes).ConclusionsWe conclude that the gene sets required for a homologous process diverge more than widely believed. Hence, the insights gained in flies may be less representative for insects or protostomes than previously thought, and work in complementary model systems is required to gain a comprehensive picture. The RNAi screening resources developed in this project, the expanding transgenic toolkit, and our large-scale functional data make T. castaneum an excellent model system in that endeavor.
Highlights
Most of the known genes required for developmental processes have been identified by genetic screens in a few well-studied model organisms, which have been considered representative of related species, and informative—to some degree—for human biology
For 30% of these genes, no functional annotation had been available at FlyBase at all such that we provide the first functional Gene Ontology (GO) assignment for the respective ortholog group in insects
Reaching the final dataset for pupal injections of the large scale iBeetle screen We added 3200 genes to the previously published 5300 genes of our large-scale iBeetle screen [17], reaching a coverage of 51% of the T. castaneum gene set of a total of 16,593 currently annotated genes [22]
Summary
Most of the known genes required for developmental processes have been identified by genetic screens in a few well-studied model organisms, which have been considered representative of related species, and informative—to some degree—for human biology. Only in a very small number of genetic model species like the mouse Mus musculus, the zebrafish Danio rerio, the nematode Caenorhabditis elegans, and the vinegar fly Drosophila melanogaster have the functions of developmental genes been assayed in systematic screens. This restriction to a few model systems is a consequence of the necessity for an elaborate genetic and molecular tool kit, which is extremely laborious to establish [1,2,3,4]. Knowing the degrees of gene function divergence is relevant for understanding the evolution of biodiversity and for applied research, e.g., for transferring knowledge from model systems to species relevant for medical applications or pest control
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