Abstract
Positional information is required for animal regeneration, yet how it is harbored in adult tissues is poorly understood. In planarians, positional control genes (PCGs) control regeneration outcomes and are regionally expressed predominately in the musculature. Acoels are early diverging bilaterally symmetric animals, having separated from other bilaterians > 550 million years ago. Here, we find that PCGs in the acoel Hofstenia miamia are expressed together and specifically in a primary differentiated cell type: muscle. The vast majority of Hofstenia muscle cells in regions tested express PCGs, suggesting positional information is a major feature of muscle. PCG expression domains are dynamic in muscle after injury, consistent with known PCG roles in guiding regeneration. These data demonstrate an instructive positional role for Hofstenia muscle and this similarity with planarians suggests mesodermal muscle originated at the base of the Bilateria not only for contraction, but also as the source of positional information guiding regeneration.
Highlights
Positional information is required for animal regeneration, yet how it is harbored in adult tissues is poorly understood
To test whether Hofstenia positional control genes (PCGs) expression was in muscle, we developed a fluorescence in situ hybridization (FISH) protocol that allowed detection of the nuclei connected to muscle fibers, involving visualizing tropomyosin messenger RNA transcripts within individual cells (Fig. 2a and Supplementary Fig. 2a–c)
Hofstenia muscle cells are organized into long fibers; dissociation of muscle fibers reveals that individual muscle cells appear to be mononucleate (Supplementary Fig. 2d)
Summary
Positional information is required for animal regeneration, yet how it is harbored in adult tissues is poorly understood. In one classical model system for studying regeneration, planarian flatworms, muscle cells have been identified as the primary site of expression of patterning genes[5] This specific expression of patterning molecules indicates that muscle is a major source of flatworm adult positional information[5]. Recent phylogenetic work using transcriptome-level sequences supports a position for the acoels, together with nemertodermatids and Xenoturbella, as a sister clade to all other bilaterians (the bilaterally symmetric animals) (Fig. 1a)[17,18,19,20,21,22] This phylogenetic placement of acoels suggests that they diverged from other bilaterians over 550 million years ago[7]. Admp sFRP-1 D fz-11 bmp V admp notum D wnt-1 notum D fz-11 sFRP-1 fz-11 admp wnt-1 bmp fz-1 notum
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