An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium
The genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2019-10-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/49065 |
| _version_ | 1828221634916384768 |
|---|---|
| author | Bicheng He Marita Buescher Max Stephen Farnworth Frederic Strobl Ernst HK Stelzer Nikolaus DB Koniszewski Dominik Muehlen Gregor Bucher |
| author_facet | Bicheng He Marita Buescher Max Stephen Farnworth Frederic Strobl Ernst HK Stelzer Nikolaus DB Koniszewski Dominik Muehlen Gregor Bucher |
| author_sort | Bicheng He |
| collection | DOAJ |
| description | The genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine animals has remained elusive. Here, we study the function of the Tc-foxQ2 forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of Tc-foxQ2 positive neural progenitor cells based on differential co-expression with Tc-six3/optix, Tc-six4, Tc-chx/vsx, Tc-nkx2.1/scro, Tc-ey, Tc-rx and Tc-fez1. An enhancer trap line built by genome editing marked Tc-foxQ2 positive neurons, which projected through the primary brain commissure and later through a subset of commissural fascicles. Eventually, they contributed to the central complex. Strikingly, in Tc-foxQ2 RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes foxQ2 as a key regulator of brain midline structures, which distinguish the protocerebrum from segmental ganglia. Unexpectedly, our data suggest that the central complex evolved by integrating neural cells from an ancestral anterior neuroendocrine center. |
| first_indexed | 2024-04-12T16:43:05Z |
| format | Article |
| id | doaj.art-310eff6f41264304b4f56456ee94b3ea |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:43:05Z |
| publishDate | 2019-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-310eff6f41264304b4f56456ee94b3ea2022-12-22T03:24:41ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.49065An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle TriboliumBicheng He0Marita Buescher1Max Stephen Farnworth2https://orcid.org/0000-0003-2418-3203Frederic Strobl3Ernst HK Stelzer4https://orcid.org/0000-0003-1545-0736Nikolaus DB Koniszewski5Dominik Muehlen6Gregor Bucher7https://orcid.org/0000-0002-4615-6401Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, GermanyJohann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, GermanyJohann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany; Göttingen Graduate Center for Molecular Biosciences, Neurosciences and Biophysics, Göttingen, GermanyBuchmann Institute for Molecular Life Sciences (BMLS), Goethe University, Frankfurt, GermanyBuchmann Institute for Molecular Life Sciences (BMLS), Goethe University, Frankfurt, GermanyJohann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, GermanyJohann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, GermanyJohann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, GermanyThe genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine animals has remained elusive. Here, we study the function of the Tc-foxQ2 forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of Tc-foxQ2 positive neural progenitor cells based on differential co-expression with Tc-six3/optix, Tc-six4, Tc-chx/vsx, Tc-nkx2.1/scro, Tc-ey, Tc-rx and Tc-fez1. An enhancer trap line built by genome editing marked Tc-foxQ2 positive neurons, which projected through the primary brain commissure and later through a subset of commissural fascicles. Eventually, they contributed to the central complex. Strikingly, in Tc-foxQ2 RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes foxQ2 as a key regulator of brain midline structures, which distinguish the protocerebrum from segmental ganglia. Unexpectedly, our data suggest that the central complex evolved by integrating neural cells from an ancestral anterior neuroendocrine center.https://elifesciences.org/articles/49065foxQ2TC004761CG11152central complexbrain commissureapical organ |
| spellingShingle | Bicheng He Marita Buescher Max Stephen Farnworth Frederic Strobl Ernst HK Stelzer Nikolaus DB Koniszewski Dominik Muehlen Gregor Bucher An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium eLife foxQ2 TC004761 CG11152 central complex brain commissure apical organ |
| title | An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium |
| title_full | An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium |
| title_fullStr | An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium |
| title_full_unstemmed | An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium |
| title_short | An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium |
| title_sort | ancestral apical brain region contributes to the central complex under the control of foxq2 in the beetle tribolium |
| topic | foxQ2 TC004761 CG11152 central complex brain commissure apical organ |
| url | https://elifesciences.org/articles/49065 |
| work_keys_str_mv | AT bichenghe anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT maritabuescher anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT maxstephenfarnworth anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT fredericstrobl anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT ernsthkstelzer anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT nikolausdbkoniszewski anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT dominikmuehlen anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT gregorbucher anancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT bichenghe ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT maritabuescher ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT maxstephenfarnworth ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT fredericstrobl ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT ernsthkstelzer ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT nikolausdbkoniszewski ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT dominikmuehlen ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium AT gregorbucher ancestralapicalbrainregioncontributestothecentralcomplexunderthecontroloffoxq2inthebeetletribolium |