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The evolutionary origins of the hypoxia-sensitive cells that trigger amniote respiratory reflexes - carotid body glomus cells, and 'pulmonary neuroendocrine cells' (PNECs) - are obscure. Homology has been proposed between glomus cells, which are neural crest-derived, and the hypoxia-sensitive 'neuroepithelial cells' (NECs) of fish gills, whose embryonic origin is unknown. NECs have also been likened to PNECs, which differentiate in situ within lung airway epithelia. Using genetic lineage-tracing and neural crest-deficient mutants in zebrafish, and physical fate-mapping in frog and lamprey, we find that NECs are not neural crest-derived, but endoderm-derived, like PNECs, whose endodermal origin we confirm. We discover neural crest-derived catecholaminergic cells associated with zebrafish pharyngeal arch blood vessels, and propose a new model for amniote hypoxia-sensitive cell evolution: endoderm-derived NECs were retained as PNECs, while the carotid body evolved via the aggregation of neural crest-derived catecholaminergic (chromaffin) cells already associated with blood vessels in anamniote pharyngeal arches.

Original publication

DOI

10.7554/eLife.21231

Type

Journal article

Journal

Elife

Publication Date

07/04/2017

Volume

6

Keywords

carotid body, chicken, developmental biology, endoderm, fate-mapping, mouse, neural crest, neuroepithelial cells, sea lamprey (Petromyzon marinus), stem cells, xenopus, zebrafish, Animals, Anura, Biological Evolution, Cell Hypoxia, Cell Lineage, Lampreys, Neuroendocrine Cells, Neuroepithelial Cells, Zebrafish