Regeneration of oral siphon pigment organs in the ascidian Ciona intestinalis

Abstract

Ascidians have powerful capacities for regeneration but the underlying mechanisms are poorly understood. Here we examine oral siphon regeneration in the solitary ascidian Ciona intestinalis. Following amputation, the oral siphon rapidly reforms oral pigment organs (OPO) at its distal margin prior to slower regeneration of proximal siphon parts. The early stages of oral siphon reformation include cell proliferation and re-growth of the siphon nerves, although the neural complex (adult brain and associated organs) is not required for regeneration. Young animals reform OPO more rapidly after amputation than old animals indicating that regeneration is age dependent. UV irradiation, microcautery, and cultured siphon explant experiments indicate that OPOs are replaced as independent units based on local differentiation of progenitor cells within the siphon, rather than by cell migration from a distant source in the body. The typical pattern of eight OPOs and siphon lobes is restored with fidelity after distal amputation of the oral siphon, but as many as 16 OPOs and lobes can be reformed following proximal amputation near the siphon base. Thus, the pattern of OPO regeneration is determined by cues positioned along the proximal distal axis of the oral siphon. A model is presented in which columns of siphon tissue along the proximal–distal axis below pre-existing OPO are responsible for reproducing the normal OPO pattern during regeneration. This study reveals previously unknown principles of oral siphon and OPO regeneration that will be important for developing Ciona as a regeneration model in urochordates, which may be the closest living relatives of vertebrates.

The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration

“…This variability actually reflects the constraints applied by both the developmental status of the organism and the pre-injury homeostatic conditions of the injured tissue on this module. Indeed the length of this module is directly influenced by the intensity of the developmental and aging processes on-going in the regenerating organism 84,85 : basically no need for a bridge between wound healing and re-development in the embryo, but a bridge that gets longer with the closing of the developmental processes and the progressive appearance of aging in the adult. Also the homeostatic status at the time and place of injury defines which cellular tools can be activated upon injury.…”

Regeneration, Stem Cells, and Aging in the Tunicate Ciona

“…Subsequently, a detailed analysis showed that the NC could be completely replaced within about a month after ablation (Schultze, 1899). Many different investigators have now confirmed NC and oral siphon regeneration and contributed additional details about the processes (Sutton, 1953;Whittaker, 1975;Bollner et al 1992Bollner et al , 1993Bollner et al , 1995Bollner et al , 1997Dahlberg et al, 2009;Auger et al, 2010). The capacity for complete regeneration from body fragments has also been investigated.…”

“…Recent studies of Ciona regeneration have focused on the oral siphon as a model (Auger et al, 2010;Jeffery, 2012;. The oral siphon is a thin muscular tube covered by tunic on its outer side ( Fig.…”

“…2A), although there are no tentacles at its base. The OPO are thought to be sensory organs (Dilly and Wolken, 1973;Auger et al, 2010), but their precise function is not understood.…”

“…Oral siphon regeneration has been separated into three steps (Auger et al, 2010). The first step is wound epidermis formation, which involves epidermal cell division to produce a new epithelium closing over the wound site (Fig.…”