Abstract
How positional information instructs adult tissue maintenance is poorly understood. Planarians undergo whole-body regeneration and tissue turnover, providing a model for adult positional information studies. Genes encoding secreted and transmembrane components of multiple developmental pathways are predominantly expressed in planarian muscle cells. Several of these genes regulate regional identity, consistent with muscle harboring positional information. Here, single-cell RNA-sequencing of 115 muscle cells from distinct anterior-posterior regions identified 44 regionally expressed genes, including multiple Wnt and ndk/FGF receptor-like (ndl/FGFRL) genes. Two distinct FGFRL-Wnt circuits, involving juxtaposed anterior FGFRL and posterior Wnt expression domains, controlled planarian head and trunk patterning. ndl-3 and wntP-2 inhibition expanded the trunk, forming ectopic mouths and secondary pharynges, which independently extended and ingested food. fz5/8-4 inhibition, like that of ndk and wntA, caused posterior brain expansion and ectopic eye formation. Our results suggest that FGFRL-Wnt circuits operate within a body-wide coordinate system to control adult axial positioning.
Highlights
Adult animals replace cells during tissue turnover and, in many cases, regeneration
The prior identification of a single, body-wide cell type expressing genes implicated in patterning in restricted domains (Witchley et al, 2013) raised the possibility that RNA sequencing of muscle cells could systematically identify components of this candidate adult positional information system
Non-dividing single cells from 10 consecutive regions along the AP axis (Figure 1A) were isolated by fluorescence activated cell sorting (FACS), and the resulting single-cell cDNA libraries were screened by qRT-PCR for expression of planarian muscle markers before sequencing (Methods, Figure 1—figure supplement 1A–C, Supplementary file 1A)
Summary
Adult animals replace cells during tissue turnover and, in many cases, regeneration. Several striking planarian phenotypes associated with altered regional tissue identity during tissue turnover have been identified, including hypercephalized (Wnt-signaling inhibition) (Petersen and Reddien, 2008; Gurley et al, 2008; Iglesias et al, 2008) and ventralized (BMP-signaling inhibition) (Reddien et al, 2007; Molina et al, 2007; Orii and Watanabe, 2007) planarians. Reminiscent of the roles of Wnt and Bmp in planarian regeneration and tissue turnover, Wnt regulates anterior-posterior (AP) axis development (Petersen and Reddien, 2009b; Niehrs, 2010) and Scimone et al eLife 2016;5:e12845.
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