Two FGFRL-Wnt circuits organize the planarian anteroposterior axis

Elife. 2016 Apr 11:5:e12845. doi: 10.7554/eLife.12845.

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.

Keywords: FGFRL; Wnt signaling; developmental biology; muscle; patterning; planarians; single cell; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Brain / anatomy & histology
  • Brain / growth & development
  • Brain / metabolism
  • Frizzled Receptors / genetics
  • Frizzled Receptors / metabolism
  • Gastrointestinal Tract / anatomy & histology
  • Gastrointestinal Tract / growth & development
  • Gastrointestinal Tract / metabolism
  • Gene Expression Regulation, Developmental
  • Helminth Proteins / genetics*
  • Helminth Proteins / metabolism
  • Muscle Cells / cytology
  • Muscle Cells / metabolism
  • Muscles / cytology
  • Muscles / metabolism
  • Planarians / anatomy & histology
  • Planarians / growth & development
  • Planarians / metabolism*
  • Receptors, Fibroblast Growth Factor / genetics*
  • Receptors, Fibroblast Growth Factor / metabolism
  • Regeneration / genetics
  • Sequence Analysis, RNA
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism
  • Signal Transduction / genetics*
  • Single-Cell Analysis
  • Wnt Proteins / genetics*
  • Wnt Proteins / metabolism
  • beta Catenin / genetics
  • beta Catenin / metabolism

Substances

  • Frizzled Receptors
  • Helminth Proteins
  • Receptors, Fibroblast Growth Factor
  • Wnt Proteins
  • beta Catenin
  • Serine Endopeptidases