Evolutionary conservation and conversion of Foxg1 function in brain development

Kumamoto, Takuma; Hanashima, Carina

doi:10.1111/dgd.12367

Cited by 90 publications

(81 citation statements)

References 88 publications

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“…In addition to the investigation of Hox genes we tested expression of several head-specific genes in the early larva (42 hpf) and advanced 8-tentacle actinotrocha. The genes, which expression we investigated, were foxG (also known as brain factor-1 or BF-1), foxQ2, six3/6, otx and pax4/6, all commonly considered as head markers (38,45,89,(93)(94)(95)(96)(97). One of the two foxG paralogues (see methods section for details), which expression we managed to detect, foxGa, is expressed in the early larva in the epidermal cells, from which the tentacles will develop (Fig.…”

Section: Head-specific Genesmentioning

confidence: 99%

Hox gene expression during development of the phoronid Phoronopsis harmeri

Gąsiorowski

Hejnol²

2020

Preprint

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Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results: We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, anterior digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions: The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a “head larva”, which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.

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Section: Head-specific Genesmentioning

confidence: 99%

Hox gene expression during development of the phoronid Phoronopsis harmeri

Gąsiorowski

Hejnol²

2020

Preprint

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“…While notably already being expressed in the SCE anterior to the ANR at the three somite stage, subsequent expression of Fgf8 in the ANR aids to induce Foxg1 expression in the anterior, Six3 + NE by the five somite stage. Once expressed in the rostral NE, Foxg1 acts to establish a permissive telencephalic progenitor field (88,237,241).…”

Section: Discussionmentioning

confidence: 99%

“…Foxg1 expression in the nascent telencephalic progenitor field has been shown to coordinate the cellular interpretation of these organizing centers (88,89,232). For instance, in the absence of functional Foxg1 the ventral telencephalon of mice cannot properly interpret ventral signaling and the BG, derived from the ganglionic eminences and the source of tangentially migrating GABAergic cortical interneurons, fails to form (113,237). Moreover, individual neural progenitor cells that lack Foxg1 cannot contribute to the ventral telencephalic progenitors and GABAergic interneurons that arise from these progenitors (113).…”

Section: Discussionmentioning

confidence: 99%

Foxg1Organizes Cephalic Ectoderm to Repress Mandibular Fate, Regulate Apoptosis, Generate Choanae, Elaborate the Auxiliary Eye and Pattern the Upper Jaw

Depew

Compagnucci

2020

Preprint

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Gnathostome jaw patterning involves focal instructive signals from the embryonic surface cephalic ectoderm (SCE) to a fungible population of cranial neural crest. The spatial refinement of these signals, particularly for those patterning the upper jaws, is not fully understood. We demonstrate that Foxg1, broadly expressed in the SCE overlying the upper jaw primordia, is required for both neurocranial and viscerocranial development, including the sensory capsules, neurocranial base, middle ear, and upper jaws. Foxg1 controls upper jaw molecular identity and morphologic development by actively inhibiting the inappropriate acquisition of lower jaw molecular identity within the upper jaw primordia, and is necessary for the appropriate elaboration of the λ-junction, choanae, palate, vibrissae, rhinarium, upper lip and auxiliary eye. It regulates intra-epithelial cellular organization, gene expression, and the topography of apoptosis within the SCE. Foxg1 integrates forebrain and skull development and genetically interacts with Dlx5 to establish a single, rostral cranial midline.

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“…In addition to the investigation of Hox genes we tested expression of several head-specific genes in the early larva (42 hpf ) and advanced 8-tentacle actinotrocha. The genes, whose expression we investigated, were foxG (also known as brain factor-1 or BF-1), foxQ2, six3/6, otx and pax4/6, all commonly considered as head markers [38,45,89,[93][94][95][96][97]. One of the two foxG paralogues Black arrowheads indicate expression in the metasomal sac, blue arrowheads expression in the protonephridia, red arrowheads expression in the mesoderm, green arrowheads expression in the telotroch and magenta arrowheads expression in the digestive system.…”

Section: Head-specific Genesmentioning

confidence: 99%

Hox gene expression during development of the phoronid Phoronopsis harmeri

Gąsiorowski

Hejnol

2020

EvoDevo

View full text Add to dashboard Cite

Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here, we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results:We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions:The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a "head larva", which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.

show abstract

Evolutionary conservation and conversion of Foxg1 function in brain development

Cited by 90 publications

References 88 publications

Hox gene expression during development of the phoronid Phoronopsis harmeri

Hox gene expression during development of the phoronid Phoronopsis harmeri

Foxg1Organizes Cephalic Ectoderm to Repress Mandibular Fate, Regulate Apoptosis, Generate Choanae, Elaborate the Auxiliary Eye and Pattern the Upper Jaw

Hox gene expression during development of the phoronid Phoronopsis harmeri

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