A key role for <i>foxQ2</i> in anterior head and central brain patterning in insects

Kitzmann, Peter; Weißkopf, Matthias; Schacht, Magdalena Ines; Bucher, Gregor

doi:10.1242/dev.147637

Cited by 26 publications

(85 citation statements)

References 74 publications

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“…Some anterior 315 aberrations stemmed from the previously described loss of the labrum (white arrows in Fig. 7A, B) 316 (Kitzmann et al, 2017). In wildtype NS15 embryos, the brain primordium had increased in size by 317 additional fascicles, the primary commissure had split and first chiasmata had formed (white arrowhead 318 in Fig.…”

mentioning

confidence: 88%

“…263 2I'). and after RNAi-knock-down of Tc-foxQ2, the CX is disturbed (Kitzmann et al, 2017). Therefore, we 267…”

Section: Introduction 60mentioning

confidence: 96%

“…1A''), a small median group (gray) and a single lateral cell (orange). These 155 groups correspond to three domains into which the Tc-foxQ2 expression splits in the neuroectoderm 156 (Kitzmann et al, 2017). At NS11, the number had decreased to 9-12 cells expressing both markers (n=6; 157 Fig.…”

Section: Introduction 60mentioning

confidence: 97%

“…Apparently, the 136 insect CX evolved by integrating cells from the ancestral anterior-most neuroectoderm, which gives rise 137 to the apical organ including the apical tuft in marine animals. Tc-foxQ2 marks neural progenitor cells with four different molecular identities 143 In the embryo, Tc-foxQ2 is expressed in the anterior neuroectoderm from earliest stages onwards 144 indicating a role in the specification of neuroblasts (Kitzmann et al, 2017). Hence, we sought to 145 determine which neural progenitor cells (NPCs) expressed Tc-foxQ2.…”

Section: Introduction 60mentioning

confidence: 99%

“…These data indicated that Tc-foxQ2 was required for survival of neural cells and that upon RNAi these 372 cells were lost by apoptosis. Indeed, increased cell death had been observed after Tc-foxQ2 RNAi at NS13 373 (Kitzmann et al, 2017). The reduced number of Tc-foxQ2 + cells was likely the reason for the thinner 374 commissure while its altered path might be a secondary effect due to general misspecification in the 375 central brain after Tc-foxQ2 RNAi (see below).…”

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confidence: 98%

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An ancestral apical brain region contributes to the central complex under the control offoxQ2in the beetleTribolium castaneum

Buescher

Farnworth

et al. 2019

Preprint

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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.Summary statementAn ancestral neuroendocrine center contributes to the evolution of the central complex. foxQ2 is a gene required for the development of midline structures of the insect brain, which distinguish protocerebrum from segmental ganglia.

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mentioning

confidence: 88%

“…263 2I'). and after RNAi-knock-down of Tc-foxQ2, the CX is disturbed (Kitzmann et al, 2017). Therefore, we 267…”

Section: Introduction 60mentioning

confidence: 96%

Section: Introduction 60mentioning

confidence: 97%

Section: Introduction 60mentioning

confidence: 99%

mentioning

confidence: 98%

See 3 more Smart Citations

An ancestral apical brain region contributes to the central complex under the control offoxQ2in the beetleTribolium castaneum

Buescher

Farnworth

et al. 2019

Preprint

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Coming into clear sight at last: Ancestral and derived events during chelicerate visual system development

Friedrich

2022

BioEssays

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Pioneering molecular work on chelicerate visual system development in the horseshoe crab Limulus polyphemus surprised with the possibility that this process may not depend on the deeply conserved retinal determination function of Pax6 transcription factors. Genomic, transcriptomic, and developmental studies in spiders now reveal that the arthropod Pax6 homologs eyeless and twin of eyeless act as ancestral determinants of the ocular head segment in chelicerates, which clarifies deep gene regulatory and structural homologies and recommends more unified terminologies in the comparison of arthropod visual systems. Following this phylotypic stage, chelicerate visual system development differs fundamentally from other arthropods during the compartmentalization of the ocular segment in that eye and optic neuropil primordia originate independently from each other. Comparative analyses of this phase identified further gene regulatory homologies but also major differences, most notably the possibly compensatory replacement of Pax6 by Pax2 in lateral eye specification. Also see the video

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cis‐Regulatory analysis for later phase of anterior neuroectoderm‐specific foxQ2 expression in sea urchin embryos

Yamazaki

Yamamoto

Yaguchi

et al. 2019

Genesis

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Summary The specification of anterior neuroectoderm is controlled by a highly conserved molecular mechanism in bilaterians. A forkhead family gene, foxQ2, is known to be one of the pivotal regulators, which is zygotically expressed in this region during embryogenesis of a broad range of bilaterians. However, what controls the expression of this essential factor has remained unclear to date. To reveal the regulatory mechanism of foxQ2, we performed cis‐regulatory analysis of two foxQ2 genes, foxQ2a and foxQ2b, in a sea urchin Hemicentrotus pulcherrimus. In sea urchin embryos, foxQ2 is initially expressed in the entire animal hemisphere and subsequently shows narrower expression restricted to the anterior pole region. In this study, as a first step to understand the foxQ2 regulation, we focused on the later restricted expression and analyzed the upstream cis‐regulatory sequences of foxQ2a and foxQ2b by using the constructs fused to short half‐life green fluorescent protein. Based on deletion and mutation analyses of both foxQ2, we identified each of the five regulatory sequences, which were 4–9 bp long. Neither of the regulatory sequences contains any motifs for ectopic activation or spatial repression, suggesting that later mRNA localization is regulated in situ. We also suggest that the three amino acid loop extension‐class homeobox gene Meis is involved in the maintenance of foxQ2b, the expression of which is dominant during embryogenesis.

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A key role for foxQ2 in anterior head and central brain patterning in insects

Cited by 26 publications

References 74 publications

An ancestral apical brain region contributes to the central complex under the control offoxQ2in the beetleTribolium castaneum

An ancestral apical brain region contributes to the central complex under the control offoxQ2in the beetleTribolium castaneum

Coming into clear sight at last: Ancestral and derived events during chelicerate visual system development

cis‐Regulatory analysis for later phase of anterior neuroectoderm‐specific foxQ2 expression in sea urchin embryos

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