Enhancer blocking and transvection at the Drosophila apterous locus

Genetics. 2008 Jan;178(1):127-43. doi: 10.1534/genetics.107.077768.

Abstract

Intra- and interchromosomal interactions have been implicated in a number of genetic phenomena in diverse organisms, suggesting that the higher-order structural organization of chromosomes in the nucleus can have a profound impact on gene regulation. In Drosophila, homologous chromosomes remain paired in somatic tissues, allowing for trans interactions between genes and regulatory elements on the two homologs. One consequence of homolog pairing is the phenomenon of transvection, in which regulatory elements on one homolog can affect the expression of a gene in trans. We report a new instance of transvection at the Drosophila apterous (ap) locus. Two different insertions of boundary elements in the ap regulatory region were identified. The boundaries are inserted between the ap wing enhancer and the ap promoter and have highly penetrant wing defects typical of mutants in ap. When crossed to an ap promoter deletion, both boundary inserts exhibit the interallelic complementation characteristic of transvection. To confirm that transvection occurs at ap, we generated a deletion of the ap wing enhancer by FRT-mediated recombination. When the wing-enhancer deletion is crossed to the ap promoter deletion, strong transvection is observed. Interestingly, the two boundary elements, which are inserted approximately 10 kb apart, fail to block enhancer action when they are present in trans to one another. We demonstrate that this is unlikely to be due to insulator bypass. The transvection effects described here may provide insight into the role that boundary element pairing plays in enhancer blocking both in cis and in trans.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • DNA Transposable Elements / genetics
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Enhancer Elements, Genetic / genetics*
  • Gene Expression Regulation*
  • Heterozygote
  • Homeodomain Proteins / genetics*
  • LIM-Homeodomain Proteins
  • Models, Genetic
  • Mutagenesis, Insertional
  • Mutation / genetics
  • Phenotype
  • Promoter Regions, Genetic / genetics
  • Repressor Proteins / genetics
  • Transcription Factors / genetics*
  • Wings, Animal / anatomy & histology

Substances

  • DNA Transposable Elements
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Homeodomain Proteins
  • LIM-Homeodomain Proteins
  • Repressor Proteins
  • Transcription Factors
  • ap protein, Drosophila
  • su(Hw) protein, Drosophila
  • z protein, Drosophila