Evolution of insect dorsoventral patterning mechanisms

Cold Spring Harb Symp Quant Biol. 2009;74:275-9. doi: 10.1101/sqb.2009.74.021. Epub 2009 Oct 20.

Abstract

The dorsoventral (DV) patterning of the early Drosophila embryo depends on Dorsal, a maternal sequence-specific transcription factor related to mammalian NF-kappaB. Dorsal controls DV patterning through the differential regulation of approximately 50 target genes in a concentration-dependent manner. Whole-genome methods, including ChIP-chip and ChIP-seq assays, have identified approximately 100 Dorsal target enhancers, and more than one-third of these have been experimentally confirmed via transgenic embryo assays. Despite differences in DV patterning among divergent insects, a number of the Dorsal target enhancers are located in conserved positions relative to the associated transcription units. Thus, the evolution of novel patterns of gene expression might depend on the modification of old enhancers, rather than the invention of new ones. As many as half of all Dorsal target genes appear to contain "shadow" enhancers: a second enhancer that directs the same or similar expression pattern as the primary enhancer. Preliminary studies suggest that shadow enhancers might help to ensure resilience of gene expression in response to environmental and genetic perturbations. Finally, most Dorsal target genes appear to contain RNA polymerase II (pol II) prior to their activation. Stalled pol II fosters synchronous patterns of gene activation in the early embryo. In contrast, DV patterning genes lacking stalled pol II are initially activated in an erratic or stochastic fashion. It is possible that stalled pol II confers fitness to a population by ensuring coordinate deployment of the gene networks controlling embryogenesis.

Publication types

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

MeSH terms

  • Animals
  • Biological Evolution*
  • Body Patterning / genetics*
  • Drosophila / embryology
  • Drosophila / genetics
  • Drosophila Proteins / genetics
  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Developmental
  • Genes, Insect
  • Insecta / embryology*
  • Insecta / genetics*
  • Nuclear Proteins / genetics
  • Phosphoproteins / genetics
  • Transcription Factors / genetics

Substances

  • Drosophila Proteins
  • Nuclear Proteins
  • Phosphoproteins
  • Transcription Factors
  • dl protein, Drosophila