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Evolution of the endothelin pathway drove neural crest cell diversification.
Square TA
,
Jandzik D
,
Massey JL
,
Romášek M
,
Stein HP
,
Hansen AW
,
Purkayastha A
,
Cattell MV
,
Medeiros DM
.
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Neural crest cells (NCCs) are migratory, multipotent embryonic cells that are unique to vertebrates and form an array of clade-defining adult features. The evolution of NCCs has been linked to various genomic events, including the evolution of new gene-regulatory networks1,2, the de novo evolution of genes3 and the proliferation of paralogous genes during genome-wide duplication events4. However, conclusive functional evidence linking new and/or duplicated genes to NCC evolution is lacking. Endothelin ligands (Edns) and endothelin receptors (Ednrs) are unique to vertebrates3,5,6, and regulate multiple aspects of NCC development in jawed vertebrates7-10. Here, to test whether the evolution of Edn signalling was a driver of NCC evolution, we used CRISPR-Cas9 mutagenesis11 to disrupt edn, ednr and dlx genes in the sea lamprey, Petromyzon marinus. Lampreys are jawless fishes that last shared a common ancestor with modern jawed vertebrates around 500 million years ago12. Thus, comparisons between lampreys and gnathostomes can identify deeply conserved and evolutionarily flexible features of vertebrate development. Using the frog Xenopus laevis to expand gnathostome phylogenetic representation and facilitate side-by-side analyses, we identify ancient and lineage-specific roles for Edn signalling. These findings suggest that Edn signalling was activated in NCCs before duplication of the vertebrate genome. Then, after one or more genome-wide duplications in the vertebrate stem, paralogous Edn pathways functionally diverged, resulting in NCC subpopulations with different Edn signalling requirements. We posit that this new developmental modularity facilitated the independent evolution of NCC derivatives in stem vertebrates. Consistent with this, differences in Edn pathway targets are associated with differences in the oropharyngeal skeleton and autonomic nervous system of lampreys and modern gnathostomes. In summary, our work provides functional genetic evidence linking the origin and duplication of new vertebrate genes with the stepwise evolution of a defining vertebrate novelty.
Aigler,
Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes.
2014, Pubmed
Aigler,
Selection and constraint underlie irreversibility of tooth loss in cypriniform fishes.
2014,
Pubmed
Asai,
Endothelin receptor type A expression defines a distinct cardiac subdomain within the heart field and is later implicated in chamber myocardium formation.
2010,
Pubmed
Baynash,
Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons.
1994,
Pubmed
Bonano,
A new role for the Endothelin-1/Endothelin-A receptor signaling during early neural crest specification.
2008,
Pubmed
,
Xenbase
Bondurand,
News from the endothelin-3/EDNRB signaling pathway: Role during enteric nervous system development and involvement in neural crest-associated disorders.
2018,
Pubmed
Braasch,
Evolution of endothelin receptors in vertebrates.
2014,
Pubmed
Braasch,
The endothelin system: evolution of vertebrate-specific ligand-receptor interactions by three rounds of genome duplication.
2009,
Pubmed
Camargo-Sosa,
Endothelin receptor Aa regulates proliferation and differentiation of Erb-dependent pigment progenitors in zebrafish.
2019,
Pubmed
Cattell,
A maternally established SoxB1/SoxF axis is a conserved feature of chordate germ layer patterning.
2012,
Pubmed
,
Xenbase
Cerny,
Evidence for the prepattern/cooption model of vertebrate jaw evolution.
2010,
Pubmed
Charité,
Role of Dlx6 in regulation of an endothelin-1-dependent, dHAND branchial arch enhancer.
2001,
Pubmed
Clouthier,
Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice.
1998,
Pubmed
Clouthier,
Regulation of facial morphogenesis by endothelin signaling: insights from mice and fish.
2010,
Pubmed
Flowers,
Highly efficient targeted mutagenesis in axolotl using Cas9 RNA-guided nuclease.
2014,
Pubmed
,
Xenbase
Fujimoto,
Non-parsimonious evolution of hagfish Dlx genes.
2013,
Pubmed
Green,
Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest.
2017,
Pubmed
Higashiyama,
On the vagal cardiac nerves, with special reference to the early evolution of the head-trunk interface.
2016,
Pubmed
Jandzik,
Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head.
2014,
Pubmed
Karne,
Cloning and characterization of an endothelin-3 specific receptor (ETC receptor) from Xenopus laevis dermal melanophores.
1993,
Pubmed
,
Xenbase
Kawasaki-Nishihara,
ET3/Ednrb2 signaling is critically involved in regulating melanophore migration in Xenopus.
2011,
Pubmed
,
Xenbase
Krauss,
Endothelin signalling in iridophore development and stripe pattern formation of zebrafish.
2014,
Pubmed
Kuraku,
Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates.
2010,
Pubmed
Kuratani,
Evolution of the vertebrate jaw from developmental perspectives.
2012,
Pubmed
Martik,
Evolution of the new head by gradual acquisition of neural crest regulatory circuits.
2019,
Pubmed
Martinez-Morales,
New genes in the evolution of the neural crest differentiation program.
2007,
Pubmed
McCauley,
Importance of SoxE in neural crest development and the evolution of the pharynx.
2006,
Pubmed
McCauley,
Conservation of Pax gene expression in ectodermal placodes of the lamprey.
2002,
Pubmed
Metallinos,
A missense mutation in the endothelin-B receptor gene is associated with Lethal White Foal Syndrome: an equine version of Hirschsprung disease.
1998,
Pubmed
Meulemans,
Gene-regulatory interactions in neural crest evolution and development.
2004,
Pubmed
Meulemans,
Id expression in amphioxus and lamprey highlights the role of gene cooption during neural crest evolution.
2003,
Pubmed
Miller,
sucker encodes a zebrafish Endothelin-1 required for ventral pharyngeal arch development.
2000,
Pubmed
Miller,
Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint.
2003,
Pubmed
Modrell,
A fate-map for cranial sensory ganglia in the sea lamprey.
2014,
Pubmed
NULL,
Drifting westward round the world.
1971,
Pubmed
Nair,
Requirements for Endothelin type-A receptors and Endothelin-1 signaling in the facial ectoderm for the patterning of skeletogenic neural crest cells in zebrafish.
2007,
Pubmed
Parichy,
Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio.
2000,
Pubmed
Ruest,
Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity.
2004,
Pubmed
Sauka-Spengler,
Ancient evolutionary origin of the neural crest gene regulatory network.
2007,
Pubmed
Session,
Genome evolution in the allotetraploid frog Xenopus laevis.
2016,
Pubmed
,
Xenbase
Simakov,
Deeply conserved synteny resolves early events in vertebrate evolution.
2020,
Pubmed
Smith,
The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution.
2018,
Pubmed
Spiewak,
Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes.
2018,
Pubmed
Square,
CRISPR/Cas9-mediated mutagenesis in the sea lamprey Petromyzon marinus: a powerful tool for understanding ancestral gene functions in vertebrates.
2015,
Pubmed
Square,
Embryonic expression of endothelins and their receptors in lamprey and frog reveals stem vertebrate origins of complex Endothelin signaling.
2016,
Pubmed
,
Xenbase
Square,
A gene expression map of the larval Xenopus laevis head reveals developmental changes underlying the evolution of new skeletal elements.
2015,
Pubmed
,
Xenbase
Stock,
Evidence from 18S ribosomal RNA sequences that lampreys and hagfishes form a natural group.
1992,
Pubmed
Sánchez-Mejías,
New roles of EDNRB and EDN3 in the pathogenesis of Hirschsprung disease.
2010,
Pubmed
Talikka,
Characterization of Xenopus Phox2a and Phox2b defines expression domains within the embryonic nervous system and early heart field.
2004,
Pubmed
,
Xenbase
Tamura,
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
2013,
Pubmed
Tavares,
Ectodermal-derived Endothelin1 is required for patterning the distal and intermediate domains of the mouse mandibular arch.
2012,
Pubmed
Thiagarajah,
Altered goblet cell differentiation and surface mucus properties in Hirschsprung disease.
2014,
Pubmed
Wang,
Targeted gene disruption in Xenopus laevis using CRISPR/Cas9.
2015,
Pubmed
,
Xenbase
Ware,
Evolutionary Conservation of the Early Axon Scaffold in the Vertebrate Brain.
2015,
Pubmed
,
Xenbase
Woodcock,
Identification of Mutant Genes and Introgressed Tiger Salamander DNA in the Laboratory Axolotl, Ambystoma mexicanum.
2017,
Pubmed
Yanagisawa,
Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene.
1998,
Pubmed
York,
An ancestral role for Semaphorin3F-Neuropilin signaling in patterning neural crest within the new vertebrate head.
2018,
Pubmed
York,
Lamprey neural crest migration is Snail-dependent and occurs without a differential shift in cadherin expression.
2017,
Pubmed
Yuan,
Gliogenesis in lampreys shares gene regulatory interactions with oligodendrocyte development in jawed vertebrates.
2018,
Pubmed
Yuan,
Neural crest and placode roles in formation and patterning of cranial sensory ganglia in lamprey.
2020,
Pubmed
Zu,
Biallelic editing of a lamprey genome using the CRISPR/Cas9 system.
2016,
Pubmed
