On the hormonal control of posterior regeneration in the annelid Platynereis dumerilii

Abstract

Regeneration is the process by which many animals are able to restore lost or injured body parts. After amputation of the posterior part of its body, the annelid Platynereis dumerilii is able to regenerate the pygidium, the posteriormost part of its body that bears the anus, and a subterminal growth zone containing stem cells that allows the subsequent addition of new segments. The ability to regenerate their posterior part (posterior regeneration) is promoted, in juvenile worms, by a hormone produced by the brain and is lost when this hormonal activity becomes low at the time the worms undergo their sexual maturation. By characterizing posterior regeneration at the morphological and molecular levels in worms that have been decapitated, we show that the presence of the head is essential for multiple aspects of posterior regeneration, as well as for the subsequent production of new segments. We also show that methylfarnesoate, the molecule proposed to be the brain hormone, can partially rescue the posterior regeneration defects observed in decapitated worms. Our results are therefore consistent with a key role of brain hormonal activity in the control of regeneration and growth in P. dumerilii, and support the hypothesis of the involvement of methylfarnesoate in this control.

Investment in regeneration versus asexual reproduction is resource‐dependent in a freshwater annelid

“…While any such variation in the frequency of injury in the wild is not well documented, injury affects sexual versus asexual reproduction to a substantially different degree in hydra (Sebestyén et al., 2018). Sexual reproducers often exhibit reduced somatic maintenance and greater senescence than asexuals, and both hydra (Miklós et al., 2021) and polychaete annelids (Álvarez‐Campos et al., 2022) exhibit near or total loss of prior regenerative ability after sexual maturation. If injury risk in the environment is significant, it may be hypothesised that P. leidyi should favour asexual reproduction accordingly, but it is unclear whether injury could contribute to selective pressure on either mode.…”

The cost and payout of age on germline regeneration and sexual maturation inPlatynereis dumerilii

“…The sesquiterpenoid methylfarnesoate (MF) was recently identified as the ’brain hormone’ in P. dumerilii (Schenk et al, 2016). MF is known to promote growth and regeneration, inhibit sexual maturation, and mediate developmental transitions in P. dumerilii and other annelids (Álvarez-Campos et al, 2023; Biggers and Laufer, 1999, 1996; Hauenschild, 1974, 1966; Hofmann, 1976; Lawrence and Soame, 2009). Brain transplantation experiments have demonstrated that the brain hormone activity generally decreases with age (Hofmann, 1976; Scully, 1964), though the exact trajectory of hormone levels over the worm’s lifetime remains unclear.…”

Annelids as models of germ cell and gonad regeneration

“…Similarly, in Platynereis, if amputation removes all the germline including the cluster of cells always located anteriorly in segments 6-8 (Fig. 3B), worms fail to regenerate the posterior body axis (Hofmann, 1966;Zelada González, 2005;Kuehn et al, 2021;Álvarez-Campos et al, 2023b). If the amputation is carried out leaving the anterior cluster intact, while removing the majority of the germline, worms regenerate the entire body along with the germ cells (Metzger et al).…”

“…Authors suggest anteriorly located vasa+ cluster of cells migrate posteriorly to regenerate gonads (de Jong & Seaver, 2017; Seaver & de Jong, 2021), though in an earlier study (Giani et al, 2011) it was suggested there is not any migration from this cell cluster (called multipotent progenitor cells or MPCs). Similarly, in Platynereis , if amputation removes all the germline including the cluster of cells always located anteriorly in segments 6–8 (Figure 3b), worms fail to regenerate the posterior body axis (Álvarez‐Campos et al, 2023b; Hofmann, 1966; Kuehn et al, 2021; Zelada González, 2005). If the amputation is carried out leaving the anterior cluster intact, while removing the majority of the germline, worms regenerate the entire body along with the germ cells (Metzger et al, in prep).…”