Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells.
At the protochordate-vertebrate transition, a new predatory lifestyle and increased body size coincided with the appearance of a true head. Characteristic innovations of this head are a skull protecting and accommodating a centralized nervous system, a jaw for prey capture and gills as respiratory organs. The neural crest (NC) is a major ontogenetic source for the 'new head' of vertebrates and its contribution to the cranial skeleton has been intensively studied in different model organisms. However, the role of NC in the expansion of the respiratory surface of the gills has been neglected. Here, we use genetic lineage labeling to address the contribution of NC to specific head structures, in particular to the gills of adult zebrafish. We generated a sox10:ER(T2)-Cre line and labeled NC cells by inducing Cre/loxP recombination with tamoxifen at embryonic stages. In juvenile and adult fish, we identified numerous established NC derivatives and, in the cranium, we precisely defined the crest/mesoderm interface of the skull roof. We show the NC origin of the opercular bones and of multiple cell types contributing to the barbels, chemosensory organs located in the mouth region. In the gills, we observed labeled primary and secondary lamellae. Clonal analysis reveals that pillar cells, a craniate innovation that mechanically supports the filaments and forms gill-specific capillaries, have a NC origin. Our data point to a crucial role for the NC in enabling more efficient gas exchange, thus uncovering a novel, direct involvement of this embryonic tissue in the evolution of respiratory systems at the protochordate-vertebrate transition.
Max-Planck-Institut für Entwicklungsbiologie, 72076 Tübingen, Germany. alessandro.mongera@tuebingen.mpg.de
Alessandro
A
Mongera
Ajeet P
AP
Singh
Mitchell P
MP
Levesque
Yi-Yen
YY
Chen
Peter
P
Konstantinidis
Christiane
C
Nüsslein-Volhard
D000818:Animals; D030801:Animals, Genetically Modified; D005075:Biological Evolution; D019070:Cell Lineage / Q000235:genetics / Q000502:physiology*; D016616:Cryoultramicrotomy; D017931:DNA Primers / Q000235:genetics; D005880:Gills / Q000166:cytology* / Q000196:embryology; D006257:Head / Q000196:embryology*; D007150:Immunohistochemistry; D019426:Integrases / Q000235:genetics; D018613:Microscopy, Confocal; D009432:Neural Crest / Q000502:physiology*; D055757:SOXE Transcription Factors / Q000235:genetics; D013629:Tamoxifen; D015027:Zebrafish / Q000196:embryology* / Q000235:genetics; D029961:Zebrafish Proteins / Q000235:genetics
D017931:DNA Primers; D055757:SOXE Transcription Factors; D029961:Zebrafish Proteins; C442229:sox10 protein, zebrafish; D013629:Tamoxifen; C045073:Cre recombinase; D019426:Integrases