Repetitive accumulation of interstitial cells generates the branched structure of Cladonema medusa tentacles.

The shaping of tissues and organs in many animals relies on interactions between the epithelial cell layer and its underlying mesoderm-derived tissues. Inductive signals, such as receptor tyrosine kinase (RTK) signaling emanating from mesoderm, act on cells of the epithelium to initiate three-dimensional changes. However, how tissues are shaped in a diploblastic animal with no mesoderm remains largely unknown. In this study, the jellyfish Cladonema pacificum was used to investigate branch formation. The tentacles on its medusa stage undergo branching, which increases the epithelial surface area available for carrying nematocytes, thereby maximizing prey capture. Pharmacological and cellular analyses of the branching process suggest a two-step model for tentacle branch formation, in which mitogen-activated protein kinase kinase signaling accumulates interstitial cells in the future branch-forming region, and fibroblast growth factor signaling regulates branch elongation. This study highlights an essential role for these pluripotent stem cells in the tissue-shaping morphogenesis of a diploblastic animal. In addition, it identifies a mechanism involving RTK signaling and cell proliferative activity at the branch tip for branching morphogenesis that is apparently conserved across the animal kingdom.

Branching pattern and morphogenesis of medusa tentacles in the jellyfish Cladonema pacificum (Hydrozoa, Cnidaria).

BACKGROUND: Branched structures are found in many natural settings, and the molecular and cellular mechanisms underlying their formation in animal development have extensively studied in recent years. Despite their importance and the accumulated knowledge from studies on several organs of Drosophila and mammals, much remains unknown about branching mechanisms in other animal species. We chose to study the jellyfish species Cladonema pacificum. Unlike many other jellyfish, this species has branched medusa tentacles, and its basal phylogenetic position in animal evolution makes it an ideal organism for studying and understanding branching morphogenesis more broadly. Branched tentacles are unique compared to other well-studied branched structures in that they have two functionally distinct identities: one with adhesive organs for attaching to a substratum, and another with nematocyst clusters for capturing prey. RESULTS: We began our analyses on C. pacificum tentacles by observing their branching during growth. We found that tentacle branches form through repeated addition of new branches to the proximal region of the main tentacle while it is elongating. At the site of branch bud formation, we observed apical thickening of the epidermal epithelial layer, possibly caused by extension of the epithelial cells along the apico-basal axis. Interestingly, tentacle branch formation required receptor tyrosine kinase signaling, which is an essential factor for branching morphogenesis in Drosophila and mammals. We also found that new branches form adhesive organs first, and then are transformed into branches with nematocyst clusters as they develop. CONCLUSIONS: These results highlight unique features in branch generation in C. pacificum medusa tentacles and illuminate conserved and fundamental mechanisms by which branched structures are created across a variety of animal species.