Notch-dependent and -independent transcription are modulated by tissue movements at gastrulation

Elife. 2022 May 18:11:e73656. doi: 10.7554/eLife.73656.

Abstract

Cells sense and integrate external information from diverse sources that include mechanical cues. Shaping of tissues during development may thus require coordination between mechanical forces from morphogenesis and cell-cell signalling to confer appropriate changes in gene expression. By live-imaging Notch-induced transcription in real time, we have discovered that morphogenetic movements during Drosophila gastrulation bring about an increase in activity-levels of a Notch-responsive enhancer. Mutations that disrupt the timing of gastrulation resulted in concomitant delays in transcription up-regulation that correlated with the start of mesoderm invagination. As a similar gastrulation-induced effect was detected when transcription was elicited by the intracellular domain NICD, it cannot be attributed to forces exerted on Notch receptor activation. A Notch-independent vnd enhancer also exhibited a modest gastrulation-induced activity increase in the same stripe of cells. Together, these observations argue that gastrulation-associated forces act on the nucleus to modulate transcription levels. This regulation was uncoupled when the complex linking the nucleoskeleton and cytoskeleton (LINC) was disrupted, indicating a likely conduit. We propose that the coupling between tissue-level mechanics, arising from gastrulation, and enhancer activity represents a general mechanism for ensuring correct tissue specification during development and that Notch-dependent enhancers are highly sensitive to this regulation.

Keywords: D. melanogaster; developmental biology; gastrulation; live-imaging; notch; tissue-mechanics; transcription.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / genetics
  • Gastrulation*
  • Gene Expression Regulation, Developmental
  • Mesoderm / metabolism
  • Morphogenesis
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism
  • Signal Transduction* / genetics

Substances

  • Receptors, Notch

Associated data

  • figshare/10.6084/m9.figshare.16619773.v45
  • figshare/10.6084/m9.figshare.19697413.v2