Vasa, PL10, and Piwi gene expression during caudal regeneration of the polychaete annelid Alitta virens

Abstract

Polychaetes are famous for their outstanding ability to regenerate lost body parts. Moreover, these worms possess a number of ancestral features in anatomy, development, and genetics, making them particularly suitable for comparative studies. Thus, fundamental as well as new undisclosed so far features of regenerative processes may be revealed, using polychaetes as a model. In the present work, we aimed to analyze the molecular basis of caudal regeneration in the nereid polychaete Alitta virens (formerly Nereis virens). We focused on homologues genes of RNA helicases Vasa and PL10 and ncRNA-binding proteins Piwi. These markers are suggested to play a significant role in maintenance of undifferentiated state of primordial germ cells and multipotent stem cells across invertebrates. In normal conditions, A. virens homologues of Vasa, PL10, and Piwi were differentially expressed in the subterminal growth zone and germline cells. Caudal amputation induced expression of studied genes de novo, which further accompanies all steps of regeneration. An early appearance of the transcripts in wound epithelium and internal blastemal cells suggests involvement of these genes in the well-known cell dedifferentiation events that assure polychaete regeneration. Provided interpretation of the gene expression dynamics implies the primary restoration of the pygidium and growth zone, which promotes following segment formation. Obtained results are valuable as a molecular fingerprint of the alterations occurring in regulatory state of locally regenerating tissues.

The Conservation of the Germline Multipotency Program, from Sponges to Vertebrates: A Stepping Stone to Understanding the Somatic and Germline Origins

“…argonaute, pl10, vasa, nanos ) in annelids and platyhelminthes (Giani et al. 2011; van Wolfswinkel 2014; Kozin and Kostyuchenko 2015). …”

Characterization of the piRNA pathway during development of the sea anemone Nematostella vectensis

“…Somatic expression of these genes seems to correlate with the ability to regenerate body parts in some animals of various phyla including the salamander Ambystoma mexicanum, 36 annelids [37][38][39][40] or planarians. 41 Cnidarians are well known for their remarkable regeneration capacity.…”

Asymmetric Distribution of pl10 and bruno2, New Members of a Conserved Core of Early Germline Determinants in Cephalochordates

“…In P. dumerilii, a number of RNA binding protein genes are expressed in PGCs as well as in putative posterior mesodermal and ectodernal stem cells during caudal regeneration, including vasa, pl10, piwi, pufA, pufB, nanos, and several tudor related genes (Rebscher et al, 2007;Gazave et al, 2013). Of these, several markers are also differentially expressed both in the germline and terminal growth zone during normal development and regeneration in the polychaetes Alitta virens and Capitella sp I (Dill and Seaver, 2008;Giani et al, 2011;Kozin and Kostyuchenko, 2015). However, the most striking example of a germline-independent redeployment of classic PGC markers in somatic tissues has been shown in the freshwater annelid Pristina leidyi, which reproduces exclusively asexually in the laboratory via paratomic fission.…”

“…By the early neurula stages, the punctate distribution may be masked by the zygotic tailbud expression (discussed below). Another dead-box containing gene, pl10, has been implicated in germ cell specification, and in some cases regeneration, from sponges to annelids (Alié et al, 2011;Rebscher et al, 2012;Leininger et al, 2014;Kozin and Kostyuchenko, 2015). PL10 is closely related phylogenetically to the Vasa protein (Kerner et al, 2011), but expression of pl10 has so far not been described in any cephalochordate.…”