Collective nuclear behavior shapes bilateral nuclear symmetry for subsequent left-right asymmetric morphogenesis in Drosophila

Development. 2021 Sep 15;148(18):dev198507. doi: 10.1242/dev.198507. Epub 2021 Apr 29.

Abstract

Proper organ development often requires nuclei to move to a specific position within the cell. To determine how nuclear positioning affects left-right (LR) development in the Drosophila anterior midgut (AMG), we developed a surface-modeling method to measure and describe nuclear behavior at stages 13-14, captured in three-dimensional time-lapse movies. We describe the distinctive positioning and a novel collective nuclear behavior by which nuclei align LR symmetrically along the anterior-posterior axis in the visceral muscles that overlie the midgut and are responsible for the LR-asymmetric development of this organ. Wnt4 signaling is crucial for the collective behavior and proper positioning of the nuclei, as are myosin II and the LINC complex, without which the nuclei fail to align LR symmetrically. The LR-symmetric positioning of the nuclei is important for the subsequent LR-asymmetric development of the AMG. We propose that the bilaterally symmetrical positioning of these nuclei may be mechanically coupled with subsequent LR-asymmetric morphogenesis.

Keywords: 3D reconstruction; Actin; Development; Image processing; Nucleus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / physiology*
  • Cell Nucleus / metabolism
  • Cell Nucleus / physiology*
  • Digestive System / metabolism
  • Digestive System / physiopathology*
  • Drosophila / metabolism
  • Drosophila / physiology*
  • Drosophila Proteins / metabolism
  • Gene Expression Regulation, Developmental / physiology
  • Morphogenesis / physiology*
  • Muscles / metabolism
  • Muscles / physiology
  • Myosin Type II / metabolism
  • Signal Transduction / physiology

Substances

  • Drosophila Proteins
  • Myosin Type II