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Benito-Gutierrez, E.

Publications and source records attributed to Benito-Gutierrez, E..

3 recordsLinked to original sources

Evolutionary dynamics of FoxQ2 transcription factors across metazoans: A tale of three ancient paralogs

FoxQ2 is a highly conserved class of Forkhead-box transcription factors expressed on the anterior side of the body in cnidarians and bilaterians. Despite this conserved expression pattern, recent phylogenetic analyses have revealed a complex and rapid evolution of this class, with several taxon-specific duplications and losses. Until recently, FoxQ2 was thought to be lost in most vertebrate lineages, and its presence and localization in different vertebrate groups remains unclear. To reconcile these conflicting reports of conservation and divergence, here we present a comprehensive analysis of the phylogenetic relationships and expression patterns of FoxQ2 genes across metazoans. By combining phylogenetics and synteny analyses of FoxQ2 sequences from 21 animal phyla, we uncover the presence of three ancient FoxQ2 paralogs in bilaterians, which we name FoxQ2a, FoxQ2b and FoxQ2c. All three FoxQ2 paralogs are present in the chordate lineage and two are conserved in vertebrates, indicating a richer repertoire of vertebrate Fox genes than previously estimated. To investigate the expression of FoxQ2 genes across bilaterians, we mined expression data from existing single cell transcriptomic datasets of mollusk, acoel, amphioxus and zebrafish development, and expanded it using fluorescent in situ hybridization in amphioxus, lamprey, skate, zebrafish and chicken. Our analysis demonstrates the conserved anterior expression of FoxQ2a and FoxQ2b paralogs while also revealing a novel domain of FoxQ2c expression within the chordate endoderm, including in amphioxus, lamprey and skate. Finally, we devise a method to predict conserved transcription factor binding sites across the three extant amphioxus genera with specificity to developmental stage and cell-type identity. This suggests conserved regulatory interactions for the expression of FoxQ2a across deuterostomes. Overall, this work clarifies the complex evolutionary history of FoxQ2 genes and identifies a newly discovered endodermally-expressed Fox gene, FoxQ2c. We further propose that the early duplication of FoxQ2a and FoxQ2b, along with their redundant functions, provided the ideal background for subfunctionalization, contributing to the fast evolutionary rate of FoxQ2 sequences observed in bilaterians.

evolutionary biology↗

A feather star is born: embryonic development and nervous system organization in the crinoid Antedon mediterranea

BackgroundCrinoids belong to the phylum Echinodermata, marine invertebrates with a highly derived pentaradial body plan. As the only living members of the Pelmatozoa, the sister group to other extant echinoderms, crinoids are in a key phylogenetic position to reconstruct the evolutionary history of this phylum. However, the development of crinoids has been scarcely investigated, limiting their potential for comparative studies. Many crinoids are difficult to collect in the wild and embryo manipulation is challenging. Conversely, the Mediterranean feather star Antedon mediterranea can be found in shallow waters and has been used for experimental studies, most notably to investigate regeneration. ResultsThe aim here was to establish A. mediterranea as an experimental system for developmental biology. To accomplish this, we set up a method for culturing embryos in vitro from zygote to hatching larva stage that allowed us to define a developmental timeline and a standardized staging system for this species. We then optimized protocols to characterize the development of the main structures of the feather star body plan, using a combination of microscopy techniques and whole mount immunohistochemistry and in situ hybridization chain reaction. Focusing on the nervous system, we show that the larval apical organ includes a combination of serotonergic, GABAergic and glutamatergic neurons that form under the influence of a conserved anterior molecular signature. The larval neural plexus is instead composed of glutamatergic neurons and develops during the formation of the ciliary bands. Larval neurons disappear at metamorphosis, and the ectoneural and entoneural components of the adult nervous system develop early in post-metamorphic stages. Furthermore, the oral ectoderm that contains the ectoneural system acquires an "anterior" signature expressing Six3/6 and Lhx2/9 orthologs. ConclusionsOur results deepen our knowledge on crinoid development and provide new techniques to investigate feather star embryogenesis, promoting the use of A. mediterranea in developmental and evolutionary biology. This in turn will pave the way for the inclusion of crinoids in comparative studies to understand the origin of the echinoderm body plan and clarify many unanswered questions on deuterostome evolution.

developmental biology↗

Rabbit Development as a Model for Single Cell Comparative Genomics

Biomedical research relies heavily on the use of model organisms to gain insight into human health and development. Traditionally, the mouse has been the favored vertebrate model, due to its experimental and genetic tractability. Non-rodent embryological studies however highlight that many aspects of early mouse development, including the egg-cylinder topology of the embryo and its method of implantation, diverge from other mammals, thus complicating inferences about human development. In this study, we constructed a morphological and molecular atlas of rabbit development, which like the human embryo, develops as a flat-bilaminar disc. We report transcriptional and chromatin accessibility profiles of almost 180,000 single cells and high-resolution histology sections from embryos spanning gastrulation, implantation, amniogenesis, and early organogenesis. Using a novel computational pipeline, we compare the transcriptional landscape of rabbit and mouse at the scale of the entire organism, revealing that extra-embryonic tissues, as well as gut and PGC cell types, are highly divergent between species. Focusing on these extra-embryonic tissues, which are highly accessible in the rabbit, we characterize the gene regulatory programs underlying trophoblast differentiation and identify novel signaling interactions involving the yolk sac mesothelium during hematopoiesis. Finally, we demonstrate how the combination of both rabbit and mouse atlases can be leveraged to extract new biological insights from sparse macaque and human data. The datasets and analysis pipelines reported here set a framework for a broader cross-species approach to decipher early mammalian development, and are readily adaptable to deploy single cell comparative genomics more broadly across biomedical research.

developmental biology↗