A Stable Thoracic Hox Code and Epimorphosis Characterize Posterior Regeneration in Capitella teleta

Danielle M De Jong,Elaine C Seaver,Michael Schubert

doi:10.1371/journal.pone.0149724

Abstract

Regeneration, the ability to replace lost tissues and body parts following traumatic injury, occurs widely throughout the animal tree of life. Regeneration occurs either by remodeling of pre-existing tissues, through addition of new cells by cell division, or a combination of both. We describe a staging system for posterior regeneration in the annelid, Capitella teleta, and use the C. teleta Hox gene code as markers of regional identity for regenerating tissue along the anterior-posterior axis. Following amputation of different posterior regions of the animal, a blastema forms and by two days, proliferating cells are detected by EdU incorporation, demonstrating that epimorphosis occurs during posterior regeneration of C. teleta. Neurites rapidly extend into the blastema, and gradually become organized into discrete nerves before new ganglia appear approximately seven days after amputation. In situ hybridization shows that seven of the ten Hox genes examined are expressed in the blastema, suggesting roles in patterning the newly forming tissue, although neither spatial nor temporal co-linearity was detected. We hypothesized that following amputation, Hox gene expression in pre-existing segments would be re-organized to scale, and the remaining fragment would express the complete suite of Hox genes. Surprisingly, most Hox genes display stable expression patterns in the ganglia of pre-existing tissue following amputation at multiple axial positions, indicating general stability of segmental identity. However, the three Hox genes, CapI-lox4, CapI-lox2 and CapI-Post2, each shift its anterior expression boundary by one segment, and each shift includes a subset of cells in the ganglia. This expression shift depends upon the axial position of the amputation. In C. teleta, thoracic segments exhibit stable positional identity with limited morphallaxis, in contrast with the extensive body remodeling that occurs during regeneration of some other annelids, planarians and acoel flatworms.

Highlights

Regeneration, the ability to replace lost tissues and body parts following traumatic injury, is present in representatives of most metazoan phyla [1,2]
A brief description of posterior regeneration in C. teleta has been published [14]; the previous study focused on reproductive adults (8 weeks post-metamorphosis), and here we provide a careful analysis of cell division patterns and blastema formation
We characterize the contribution of tissue remodeling and formation of new tissue during posterior regeneration in C. teleta

Summary

Introduction

Regeneration, the ability to replace lost tissues and body parts following traumatic injury, is present in representatives of most metazoan phyla [1,2]. In some animals, this ability is limited to the replacement of a particular cell type, tissue or structure Variation in regeneration ability exists, the widespread phylogenetic distribution of some form of regenerative capability in the Metazoa suggests an evolutionary ancient origin of regeneration with subsequent multiple losses across many lineages. Epimorphosis occurs when cell proliferation leads to formation of new tissue, while morphallaxis is characterized by re-patterning of existing tissue, in the absence of cell proliferation [3]. The broad phylogenetic distribution of documented examples of morphallaxis suggests that this might be a more widespread phenomenon than previously appreciated

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