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Activation of Hox genes during caudal regeneration of the polychaete annelid Platynereis dumerilii

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Abstract

The capability of regenerating posterior segments and pygidial structures is ancestral for annelids and has been lost only a few times within this phylum. As one of the three major segmented taxa, annelids enable us to monitor reconstruction of lost tissues and organs. During regeneration, regional identities have to be imprinted onto the newly formed segments. In this study, we show spatial and temporal localization of expression of nine Hox genes during caudal regeneration of the polychaete annelid Platynereis dumerilii. Hox genes are homeodomain genes encoding transcriptional regulators of axial patterning in bilaterian animals during development. We demonstrate that five Platynereis Hox genes belonging to paralog groups (PG) 1, 4, 5, 6, and 9–14 are expressed in domains of the regenerating nervous system consistent with providing positional information along the anteroposterior axis of the regenerate. We report that expression in regenerating neuromeres is limited to varying subsets of perikarya, called gangliosomes. Four of nine genes analyzed do not appear to be involved in axial patterning. Two genes, Pdu-Hox2 and Pdu-Hox3, are predominantly expressed in the growth zone region. For some Hox genes expression in newly formed coelomic epithelia can be observed. Platynereis Hox genes do not exhibit temporal or spatial colinearity. Although there are some similarities to previously reported expression patterns during larval and postlarval development in Nereididae (Kulakova et al. 2007), expression patterns observed during caudal regeneration also show unique patterns.

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Acknowledgements

The authors thank Brigitte Fronk and Sabine Wagner for maintenance of the Platynereis dumerilii culture and technical assistance. We gratefully acknowledge Elaine C. Seaver for the careful reading and valuable remarks. Thanks are due to unknown reviewers for valuable comments. This research was supported in part by the National Science Foundation through TeraGrid resources provided by the CIPRES portal.

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Authors and Affiliations

  1. Institut für Allgemeine und Spezielle Zoologie, Abteilung Entwicklungsbiologie, Justus-Liebig-Universität Gießen, Stephanstr.24, 35390, Gießen, Germany

    Kathrin Pfeifer, Adriaan W. C. Dorresteijn & Andreas C. Fröbius

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  1. Kathrin Pfeifer
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  2. Adriaan W. C. Dorresteijn
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  3. Andreas C. Fröbius
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Correspondence to Andreas C. Fröbius.

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Communicated by M. Martindale

K. Pfeifer and A. C. Fröbius contributed equally to this work.

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Fig. S1

Orthology assignments for Platynereis dumerilii Hox genes. Platynereis dumerilii Hox sequences are delimited by arrows. Numbers above branches indicate Bayesian posterior probabilities. Ovals delimit bootstrap support >50 at a node from either neighbor-joining (NJ) or maximum likelyhood (ML) analyses and squares show bootstrap support >50 from both NJ and ML analyses (JPEG 102 kb)

High resolution image (TIFF 639 kb)

Fig. S2

Comparison of spatial expression of Hox genes of Platynereis dumerilii in adult posterior ends and during caudal regeneration. Lighter and darker colors indicate lower and higher expression levels, respectively. The red dashed line marks the amputation site for regenerates. The asterisk marks the last original segment for regenerates. nsz nascent segment zone, pgz posterior growth zone region, py pygidium (JPEG 40 kb)

High resolution image (TIFF 950 kb)

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Pfeifer, K., Dorresteijn, A.W.C. & Fröbius, A.C. Activation of Hox genes during caudal regeneration of the polychaete annelid Platynereis dumerilii . Dev Genes Evol 222, 165–179 (2012). https://doi.org/10.1007/s00427-012-0402-z

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