Release and spread of Wingless is required to pattern the proximo-distal axis of Drosophila renal tubules

Elife. 2018 Aug 10:7:e35373. doi: 10.7554/eLife.35373.

Abstract

Wingless/Wnts are signalling molecules, traditionally considered to pattern tissues as long-range morphogens. However, more recently the spread of Wingless was shown to be dispensable in diverse developmental contexts in Drosophila and vertebrates. Here we demonstrate that release and spread of Wingless is required to pattern the proximo-distal (P-D) axis of Drosophila Malpighian tubules. Wingless signalling, emanating from the midgut, directly activates odd skipped expression several cells distant in the proximal tubule. Replacing Wingless with a membrane-tethered version that is unable to diffuse from the Wingless producing cells results in aberrant patterning of the Malpighian tubule P-D axis and development of short, deformed ureters. This work directly demonstrates a patterning role for a released Wingless signal. As well as extending our understanding about the functional modes by which Wnts shape animal development, we anticipate this mechanism to be relevant to patterning epithelial tubes in other organs, such as the vertebrate kidney.

Keywords: D. melanogaster; Malpighian tubule; Wnt/Wingless; developmental biology; morphogen; organogenesis; proximo-distal patterning; renal tubule.

Publication types

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

MeSH terms

  • Animals
  • Body Patterning*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / physiology*
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / physiology
  • Gene Expression Regulation, Developmental*
  • Kidney Tubules, Distal / embryology
  • Kidney Tubules, Distal / physiology*
  • Kidney Tubules, Proximal / embryology
  • Kidney Tubules, Proximal / physiology*
  • Morphogenesis
  • Wnt Signaling Pathway
  • Wnt1 Protein / genetics
  • Wnt1 Protein / metabolism*

Substances

  • Drosophila Proteins
  • Wnt1 Protein
  • wg protein, Drosophila