Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes
Abstract Background 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. The fruit fly Drosophila mel...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-02-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01231-4 |
| _version_ | 1818977021102915584 |
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| author | Muhammad Salim Hakeemi Salim Ansari Matthias Teuscher Matthias Weißkopf Daniela Großmann Tobias Kessel Jürgen Dönitz Janna Siemanowski Xuebin Wan Dorothea Schultheis Manfred Frasch Siegfried Roth Michael Schoppmeier Martin Klingler Gregor Bucher |
| author_facet | Muhammad Salim Hakeemi Salim Ansari Matthias Teuscher Matthias Weißkopf Daniela Großmann Tobias Kessel Jürgen Dönitz Janna Siemanowski Xuebin Wan Dorothea Schultheis Manfred Frasch Siegfried Roth Michael Schoppmeier Martin Klingler Gregor Bucher |
| author_sort | Muhammad Salim Hakeemi |
| collection | DOAJ |
| description | Abstract Background 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. 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. Results Here, 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). Conclusions We 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. |
| first_indexed | 2024-12-20T16:21:07Z |
| format | Article |
| id | doaj.art-f958f28f3e5f489d8ea8a8d99b722eb3 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-20T16:21:07Z |
| publishDate | 2022-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-f958f28f3e5f489d8ea8a8d99b722eb32022-12-21T19:33:38ZengBMCBMC Biology1741-70072022-02-0120111310.1186/s12915-022-01231-4Screens in fly and beetle reveal vastly divergent gene sets required for developmental processesMuhammad Salim Hakeemi0Salim Ansari1Matthias Teuscher2Matthias Weißkopf3Daniela Großmann4Tobias Kessel5Jürgen Dönitz6Janna Siemanowski7Xuebin Wan8Dorothea Schultheis9Manfred Frasch10Siegfried Roth11Michael Schoppmeier12Martin Klingler13Gregor Bucher14Johann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergInstitute for Zoology/Developmental Biology, University of Cologne, BiocenterDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergDepartment of Biology, Friedrich-Alexander-University Erlangen-NürnbergJohann-Friedrich-Blumenbach-Institut, GZMB, University of GöttingenAbstract Background 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. 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. Results Here, 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). Conclusions We 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.https://doi.org/10.1186/s12915-022-01231-4Gene functionComparative genomicsRNAi screeniBeetleTribolium castaneumDrosophila melanogaster |
| spellingShingle | Muhammad Salim Hakeemi Salim Ansari Matthias Teuscher Matthias Weißkopf Daniela Großmann Tobias Kessel Jürgen Dönitz Janna Siemanowski Xuebin Wan Dorothea Schultheis Manfred Frasch Siegfried Roth Michael Schoppmeier Martin Klingler Gregor Bucher Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes BMC Biology Gene function Comparative genomics RNAi screen iBeetle Tribolium castaneum Drosophila melanogaster |
| title | Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| title_full | Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| title_fullStr | Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| title_full_unstemmed | Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| title_short | Screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| title_sort | screens in fly and beetle reveal vastly divergent gene sets required for developmental processes |
| topic | Gene function Comparative genomics RNAi screen iBeetle Tribolium castaneum Drosophila melanogaster |
| url | https://doi.org/10.1186/s12915-022-01231-4 |
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