Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs.

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Autores principales: Gattoni, Giacomo, Lin, Che-Yi, York, Joshua R, Shew, Colin, Keitley, Daniel, LaBonne, Carole, Yu, Jr-Kai, Gillis, J Andrew, Benito-Gutiérrez, Elia
Formato: Artículo científico
Lenguaje:en
Publicado: Communications biology 2025
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author Gattoni, Giacomo
Lin, Che-Yi
York, Joshua R
Shew, Colin
Keitley, Daniel
LaBonne, Carole
Yu, Jr-Kai
Gillis, J Andrew
Benito-Gutiérrez, Elia
author_facet Gattoni, Giacomo
Lin, Che-Yi
York, Joshua R
Shew, Colin
Keitley, Daniel
LaBonne, Carole
Yu, Jr-Kai
Gillis, J Andrew
Benito-Gutiérrez, Elia
Gattoni, Giacomo
Lin, Che-Yi
York, Joshua R
Shew, Colin
Keitley, Daniel
LaBonne, Carole
Yu, Jr-Kai
Gillis, J Andrew
Benito-Gutiérrez, Elia
collection PubMed - marine biology
contents Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs. Gattoni, Giacomo Lin, Che-Yi York, Joshua R Shew, Colin Keitley, Daniel LaBonne, Carole Yu, Jr-Kai Gillis, J Andrew Benito-Gutiérrez, Elia Animals Forkhead Transcription Factors Evolution, Molecular Phylogeny Synteny FoxQ2 is a highly conserved Forkhead-box transcription factor expressed anteriorly in cnidarians and bilaterians, yet its evolution is marked by rapid divergence and lineage-specific duplications or losses. Moreover, its presence and localization in vertebrate groups remains unclear. To reconcile these conflicting reports of conservation and divergence, we combine phylogenetic and synteny analyses of FoxQ2 sequences from 21 animal phyla. We uncover three ancient FoxQ2 paralogs in bilaterians-FoxQ2I, FoxQ2II, and FoxQ2III. All three were present in the chordate ancestor, and two are retained in vertebrates, indicating a richer FoxQ2 repertoire in vertebrates than previously recognized. To assess FoxQ2 expression, we analyzed mollusk, acoel, amphioxus, and zebrafish single-cell transcriptomic datasets, and conducted fluorescent in situ hybridization in amphioxus, lamprey, skate, zebrafish, and chicken. FoxQ2I and FoxQ2II show conserved anterior expression, while FoxQ2III is expressed in the gut endoderm in chordates, including amphioxus, lamprey, and skate. We also predict conserved transcription factor binding sites across amphioxus genera, revealing stage- and cell-type-specific regulatory interactions for FoxQ2I in deuterostomes. Overall, this work clarifies FoxQ2's evolutionary history, identifies the endodermally expressed paralog FoxQ2III, and proposes that early duplication of FoxQ2I/II enabled subfunctionalization, driving the fast evolutionary rate of FoxQ2 sequences observed in bilaterians.
format Artículo científico
id pubmed_41423499
institution PubMed
language en
publishDate 2025
publisher Communications biology
record_format pubmed
spellingShingle Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs.
Gattoni, Giacomo
Lin, Che-Yi
York, Joshua R
Shew, Colin
Keitley, Daniel
LaBonne, Carole
Yu, Jr-Kai
Gillis, J Andrew
Benito-Gutiérrez, Elia
Animals
Forkhead Transcription Factors
Evolution, Molecular
Phylogeny
Synteny
Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs. Gattoni, Giacomo Lin, Che-Yi York, Joshua R Shew, Colin Keitley, Daniel LaBonne, Carole Yu, Jr-Kai Gillis, J Andrew Benito-Gutiérrez, Elia Animals Forkhead Transcription Factors Evolution, Molecular Phylogeny Synteny FoxQ2 is a highly conserved Forkhead-box transcription factor expressed anteriorly in cnidarians and bilaterians, yet its evolution is marked by rapid divergence and lineage-specific duplications or losses. Moreover, its presence and localization in vertebrate groups remains unclear. To reconcile these conflicting reports of conservation and divergence, we combine phylogenetic and synteny analyses of FoxQ2 sequences from 21 animal phyla. We uncover three ancient FoxQ2 paralogs in bilaterians-FoxQ2I, FoxQ2II, and FoxQ2III. All three were present in the chordate ancestor, and two are retained in vertebrates, indicating a richer FoxQ2 repertoire in vertebrates than previously recognized. To assess FoxQ2 expression, we analyzed mollusk, acoel, amphioxus, and zebrafish single-cell transcriptomic datasets, and conducted fluorescent in situ hybridization in amphioxus, lamprey, skate, zebrafish, and chicken. FoxQ2I and FoxQ2II show conserved anterior expression, while FoxQ2III is expressed in the gut endoderm in chordates, including amphioxus, lamprey, and skate. We also predict conserved transcription factor binding sites across amphioxus genera, revealing stage- and cell-type-specific regulatory interactions for FoxQ2I in deuterostomes. Overall, this work clarifies FoxQ2's evolutionary history, identifies the endodermally expressed paralog FoxQ2III, and proposes that early duplication of FoxQ2I/II enabled subfunctionalization, driving the fast evolutionary rate of FoxQ2 sequences observed in bilaterians.
title Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs.
topic Animals
Forkhead Transcription Factors
Evolution, Molecular
Phylogeny
Synteny
url https://pubmed.ncbi.nlm.nih.gov/41423499/