Whole-body regeneration and polarity repatterning in polyps of Xenia umbellata (Octocorallia)
Abstract
Cnidarians are renowned for their regenerative abilities, up to extreme whole-body regeneration (WBR), which supports recovery from disturbances and contributes to their ecological success. However, most mechanistic insight into morphogenesis and polarity in WBR still derives from cnidarian solitary polyp models. As such, WBR and polarity repatterning in polyps of colonial cnidarians, especially octocorals, is largely understudied. The pulsating zooxanthellate octocoral Xenia umbellata is increasingly recognized for its ecological resilience and invasive potential, with regenerative abilities that may contribute to its spreading success. Here, we experimentally evaluated regeneration from miniature fragments of both tentacles and polyp bodies and assessed polarity repatterning following double amputation of polyps, removing both oral and basal structures. We show that X. umbellata exhibits extreme WBR, regenerating complete polyps from fragments as small as ~0.1 mm². Regeneration from both polyp parts proceeded through a conserved sequence of stages, including tissue ball formation, ultimately producing fully functional polyps. Early regeneration dynamics differed between fragment types: tentacle-derived fragments required structural reorganization, including the initial elimination of differentiated tentacle structural features and de novo mesentery formation, whereas polyp body fragments retained their internal architecture and regenerated more rapidly. Fragment size had only a limited effect on regeneration success and rate of both polyp parts. All successful regeneration led to pulsating polyps with oral disc diameters 5-10% the size of original polyps. In contrast to solitary cnidarians, over 60% of double-amputated X. umbellata polyps regenerated two oral discs. However, non-synchronized timing of oral disc formation and biased placement of attachment discs revealed partial retention of original positional information despite loss of axial landmarks. Together, these findings suggest that regeneration in X. umbellata combines internal polarity cues with additional colony-level patterning processes absent from solitary models. The findings expand the comparative framework of cnidarian regeneration and further establish X. umbellata as a powerful model for studying WBR, polarity, and coloniality in cnidarians.