Nerves and availability of mesodermal cells are essential for the function of the segment addition zone (SAZ) during segment regeneration in polychaete annelids

Abstract

Most of annelids grow all over their asexual life through the continuous addition of segments from a special zone called "segment addition zone" (SAZ) adjacent to the posterior extremity called pygidium. Amputation of posterior segments leads to regeneration (posterior regeneration-PR) of the pygidium and a new SAZ, as well as new segments issued from this new SAZ. Amputation of anterior segments leads some species to regeneration (anterior regeneration-AR) of the prostomium and a SAZ which produces new segments postero-anteriorly as during PR. During the 1960s and 1970s decades, experimental methods on different species (Syllidae, Nereidae, Aricidae) showed that the function of SAZ depends on the presence and number of mesodermal regeneration cells. Selective destruction of mesodermal regeneration cells in AR had no effect on the regeneration of the prostomium, but as for PR, it inhibited segment regeneration. Thus, worms deprived of mesodermal regeneration cells are always able to regenerate the pygidium or the prostomium, but they are unable to regenerate segments, a result which indicates that the SAZ functions only if these regeneration cells are present during PR or AR. Additionally, during AR, nerve fibres regenerate from the cut nerve cord toward the newformed brain, a situation which deprives the SAZ of local regenerating nerve fibres and their secreted growth factors. In contrast, during PR, nerve fibres regenerate both during the entire regeneration phase and then in normal growth. This review summarizes the experimental evidence for mesoderm cell involvement in segment regeneration, and the differential impact of the digestive tube and the regenerated nerve cord during PR vs AR.

Keywords: Aricidae; Cell proliferation; Nereidae; Nerve dependence; Regeneration; Regeneration cell; Segment regeneration; Syllidae.

Fig. 1

A Schematic drawing representing a Polychaete annelid (Nereis sp. dorsal view) showing, antero-posteriorly, the prostomium (with its 2 antennae, 2 palps and 4 eyes), the peristomium (with its 4 pairs of tentacular cirri), and the following setigerous segments (with each a pair of parapodia characterized by a pair of cirri and bristles), which extends until the last part of the worm corresponding to pygidium (with its 2 anal cirri). B Posterior regenerate (ventrolateral view) of Hediste diversicolor (formerly Nereis diversicolor) 25 dpa (SEM picture) composed of the pygidium with its 2 anal cirri and 7 differentiating setigerous segments (indicated by arrows); the last one, close to the pygidium, shows only the first stage of differentiation as a bulge corresponding to the future parapodium. The space between this last differentiating segment and the pygidium corresponds to the SAZ. The SAZ is localized between the pygidium and the first sign of metamerization. C Posterior regenerate (ventral view) of decerebrated Hediste diversicolor 40 dpa; only the pygidium is completely regenerated but the presence of a pair of bulges (arrows) corresponding to the first phase of segmentation indicates that this regeneration phase fails. The dotted line indicates the limit of the regenerated area. D, E Mesodermal regeneration cells (Syllis amica). Partial view of the coelomic epithelium surrounding the intestine in the amputated segment (2 dpa) showing their swelling (double arrow in E) compared to their flat aspect in non-injured segments (single arrow in D) i: intestine. F Postero-ventral extremity of the blastema 3 dpa (PR) close to the regenerated nerve cord (n) between the mesodermal regeneration cell mass (m) and the regenerated epidermis (e); activated mesodermal cells (arrow) close to the regenerated nerves (asterisk). A modified from Boilly et al. (1975); B and C modified from Boilly (1974); D and E modified from Boilly (1967a). Scale bars 200 μm (B, C), 5 μm (D–F)

Fig. 2

A Schematic drawing representing anterior and posterior regeneration of syllids from a midbody cutting area; SAZ, segment addition zone; arrows indicating the direction of regeneration from each SAZ. B Anterior end of Syllis malaquini showing by transparency the complex anatomy of the anterior digestive tube of stomodeal origin (a specificity of Syllis) composed of 3 parts: pharynx (ph), proventricle (pr), ventricle (vc). The head (an, antenna; ey, eye; pl, palp; tc, tentacular cirri), first segments (dc, dorsal cirrus; pa, parapodium) and posterior body part (not shown in this picture) are similar to Nereis. C Anterior regenerate of Typosyllis antoni (10 dpa), limited to prostomium and peristomium (no setigerous segments regenerated) and incomplete intestine (proventricle and pharynx missing). D Normal posterior regenerate of Typosyllis antoni (10 dpa). E Anterior regenerate of Syllis amica (20 dpa), prostomium, peristomium regenerated as well 2 setigerous segments but incomplete intestine (proventricle and pharynx missing). The intestine (i, black) did not regenerate and did not penetrate into the regenerate. F Normal posterior regenerate of Syllis amica (12 dpa), the intestine (i) is regenerated towards the pygidium. G Anterior regenerate of Syllis gracilis (dorsal view) (16 dpa) composed of prostomium, peristomium and 8 setigerous regenerated segments. Note that the intestine (i) present inside the regenerate is extended anteriorly by the regenerated anterior digestive tube (of stomodeal origin) composed of (not black): pharynx (ph), proventricle (pr) and ventricle with caeca (vc). H Anterior regenerate of Syllis malaquini (18 dpa) composed of prostomium, peristomium and 7 setigerous segments with pharynx (ph) and proventricle (pr). A modified from Ribeiro et al. (2018); B from Ribeiro et al. (2020); C and D from Weidhase et al. (2017); E and F from Boilly (1967a); G from Boilly and Thibaut (1974); H picture taken by Vanessa Spieß. Scale bars 1 mm (B), 100 μm (C, D), 50 μm (E–G), 200 μm (H)