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Main Authors: Thiruppathy, Mathi, Teubner, Lauren, Roberts, Ryan R, Lasser, Micaela C, Moscatello, Alessandra, Chen, Ya-Wen, Hochstim, Christian, Ruffins, Seth, Sarkar, Arijita, Tassey, Jade, Evseenko, Denis, Lozito, Thomas P, Willsey, Helen Rankin, Gillis, J Andrew, Crump, J Gage
Format: Artículo científico
Language:en
Published: Nature 2025
Subjects:
Online Access:https://pubmed.ncbi.nlm.nih.gov/39788155/
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author Thiruppathy, Mathi
Teubner, Lauren
Roberts, Ryan R
Lasser, Micaela C
Moscatello, Alessandra
Chen, Ya-Wen
Hochstim, Christian
Ruffins, Seth
Sarkar, Arijita
Tassey, Jade
Evseenko, Denis
Lozito, Thomas P
Willsey, Helen Rankin
Gillis, J Andrew
Crump, J Gage
author_facet Thiruppathy, Mathi
Teubner, Lauren
Roberts, Ryan R
Lasser, Micaela C
Moscatello, Alessandra
Chen, Ya-Wen
Hochstim, Christian
Ruffins, Seth
Sarkar, Arijita
Tassey, Jade
Evseenko, Denis
Lozito, Thomas P
Willsey, Helen Rankin
Gillis, J Andrew
Crump, J Gage
Thiruppathy, Mathi
Teubner, Lauren
Roberts, Ryan R
Lasser, Micaela C
Moscatello, Alessandra
Chen, Ya-Wen
Hochstim, Christian
Ruffins, Seth
Sarkar, Arijita
Tassey, Jade
Evseenko, Denis
Lozito, Thomas P
Willsey, Helen Rankin
Gillis, J Andrew
Crump, J Gage
collection PubMed - marine biology
contents Repurposing of a gill gene regulatory program for outer-ear evolution. Thiruppathy, Mathi Teubner, Lauren Roberts, Ryan R Lasser, Micaela C Moscatello, Alessandra Chen, Ya-Wen Hochstim, Christian Ruffins, Seth Sarkar, Arijita Tassey, Jade Evseenko, Denis Lozito, Thomas P Willsey, Helen Rankin Gillis, J Andrew Crump, J Gage Animals Humans Biological Evolution Cartilage Ear Enhancer Elements, Genetic Gene Expression Regulation, Developmental Gills Homeodomain Proteins Transcription Factors Zebrafish How new structures emerge during evolution has long fascinated biologists. An example is how the diminutive bones of the mammalian middle ear arose from ancestral fish jawbones. By contrast, the evolutionary origin of the outer ear, another mammalian innovation, remains a mystery, partly because it is supported by non-mineralized elastic cartilage, which is rarely recovered in fossils. Whether the outer ear arose de novo or through the reuse of ancestral developmental programs has remained unknown. Here we show that the outer ear shares gene regulatory programs with the gills of fishes and amphibians for both its initial outgrowth and the later development of the elastic cartilage. Comparative single-nucleus multiomics of the human outer ear and zebrafish gills reveals conserved gene expression and putative enhancers enriched for common transcription factor binding motifs. This is reflected by the transgenic activity of human outer-ear enhancers in gills, and of fish gill enhancers in the outer ear. Furthermore, single-cell multiomics of the cartilaginous book gills of horseshoe crabs reveals a developmental program shared with the distal-less homeobox (DLX)-mediated gill program of vertebrates, with a book-gill distal-less enhancer driving expression in zebrafish gills. We propose that elements of an invertebrate gill program were reutilized in vertebrates to generate first gills and then the outer ear.
format Artículo científico
id pubmed_39788155
institution PubMed
language en
publishDate 2025
publisher Nature
record_format pubmed
spellingShingle Repurposing of a gill gene regulatory program for outer-ear evolution.
Thiruppathy, Mathi
Teubner, Lauren
Roberts, Ryan R
Lasser, Micaela C
Moscatello, Alessandra
Chen, Ya-Wen
Hochstim, Christian
Ruffins, Seth
Sarkar, Arijita
Tassey, Jade
Evseenko, Denis
Lozito, Thomas P
Willsey, Helen Rankin
Gillis, J Andrew
Crump, J Gage
Animals
Humans
Biological Evolution
Cartilage
Ear
Enhancer Elements, Genetic
Gene Expression Regulation, Developmental
Gills
Homeodomain Proteins
Transcription Factors
Zebrafish
Repurposing of a gill gene regulatory program for outer-ear evolution. Thiruppathy, Mathi Teubner, Lauren Roberts, Ryan R Lasser, Micaela C Moscatello, Alessandra Chen, Ya-Wen Hochstim, Christian Ruffins, Seth Sarkar, Arijita Tassey, Jade Evseenko, Denis Lozito, Thomas P Willsey, Helen Rankin Gillis, J Andrew Crump, J Gage Animals Humans Biological Evolution Cartilage Ear Enhancer Elements, Genetic Gene Expression Regulation, Developmental Gills Homeodomain Proteins Transcription Factors Zebrafish How new structures emerge during evolution has long fascinated biologists. An example is how the diminutive bones of the mammalian middle ear arose from ancestral fish jawbones. By contrast, the evolutionary origin of the outer ear, another mammalian innovation, remains a mystery, partly because it is supported by non-mineralized elastic cartilage, which is rarely recovered in fossils. Whether the outer ear arose de novo or through the reuse of ancestral developmental programs has remained unknown. Here we show that the outer ear shares gene regulatory programs with the gills of fishes and amphibians for both its initial outgrowth and the later development of the elastic cartilage. Comparative single-nucleus multiomics of the human outer ear and zebrafish gills reveals conserved gene expression and putative enhancers enriched for common transcription factor binding motifs. This is reflected by the transgenic activity of human outer-ear enhancers in gills, and of fish gill enhancers in the outer ear. Furthermore, single-cell multiomics of the cartilaginous book gills of horseshoe crabs reveals a developmental program shared with the distal-less homeobox (DLX)-mediated gill program of vertebrates, with a book-gill distal-less enhancer driving expression in zebrafish gills. We propose that elements of an invertebrate gill program were reutilized in vertebrates to generate first gills and then the outer ear.
title Repurposing of a gill gene regulatory program for outer-ear evolution.
topic Animals
Humans
Biological Evolution
Cartilage
Ear
Enhancer Elements, Genetic
Gene Expression Regulation, Developmental
Gills
Homeodomain Proteins
Transcription Factors
Zebrafish
url https://pubmed.ncbi.nlm.nih.gov/39788155/