Abstract
Regeneration requires both potential and instructions for tissue replacement. In planarians, pluripotent stem cells have the potential to produce all new tissue. The identities of the cells that provide regeneration instructions are unknown. Here, we report that position control genes (PCGs) that control regeneration and tissue turnover are expressed in a subepidermal layer of nonneoblast cells. These subepidermal cells coexpress many PCGs. We propose that these subepidermal cells provide a system of body coordinates and positional information for regeneration, and identify them to be muscle cells of the planarian body wall. Almost all planarian muscle cells express PCGs, suggesting a dual function: contraction and control of patterning. PCG expression is dynamic in muscle cells after injury, even in the absence of neoblasts, suggesting that muscle is instructive for regeneration. We conclude that planarian regeneration involves two highly flexible systems: pluripotent neoblasts that can generate any new cell type and muscle cells that provide positional instructions for the regeneration of any body region.
Highlights
Cellular models for regeneration must explain two essential attributes of adult tissues: the potential for regeneration and the information to guide regeneration
Positional information is essential for maintaining regional tissue identity during tissue turnover and wound repair in most adult animals, but it remains poorly understood
Adult tissue identity could be retained during tissue turnover by cell populations that autonomously maintain their regional identity
Summary
Cellular models for regeneration must explain two essential attributes of adult tissues: the potential for regeneration and the information to guide regeneration. Wnt genes are expressed in both epithelial layers near the Hydra head, and Wnt signaling promotes Hydra head regeneration (Broun et al, 2005; Hobmayer et al, 2000; Lengfeld et al, 2009) Despite these advances, how positional identities are established, maintained, and regenerated in adult tissues is poorly understood. Planarians are flatworms and constitute a classic regeneration model system (Reddien and Sánchez Alvarado, 2004) They can regenerate any missing body part and maintain adult tissues by replacing aging differentiated cells. RNA (mRNA) gradient on the dorsal side (Orii et al, 1998), and RNAi of bmp causes ventralization (Molina et al, 2007; Orii and Watanabe, 2007; Reddien et al, 2007) In all of these cases, the site of PCG expression corresponds to the body region that is affected by RNAi of that gene.
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