An adaptive transposable element insertion in the regulatory region of the EO gene in the domesticated silkworm, Bombyx mori

Mol Biol Evol. 2014 Dec;31(12):3302-13. doi: 10.1093/molbev/msu261. Epub 2014 Sep 10.

Abstract

Although there are many studies to show a key role of transposable elements (TEs) in adaptive evolution of higher organisms, little is known about the molecular mechanisms. In this study, we found that a partial TE (Taguchi) inserted in the cis-regulatory region of the silkworm ecdysone oxidase (EO) gene, which encodes a crucial enzyme to reduce the titer of molting hormone (20-hydroxyecdysone, 20E). The TE insertion occurred during domestication of silkworm and the frequency of the TE insertion in the domesticated silkworm (Bombyx mori) is high, 54.24%. The linkage disequilibrium in the TE inserted strains of the domesticated silkworm was elevated. Molecular population genetics analyses suggest that this TE insertion is adaptive for the domesticated silkworm. Luminescent reporter assay shows that the TE inserted in the cis-regulatory region of the EO gene functions as a 20E-induced enhancer of the gene expression. Further, phenotypic bioassay indicates that the silkworm with the TE insertion exhibited more stable developmental phenotype than the silkworm without the TE insertion when suffering from food shortage. Thus, the inserted TE in the cis-regulatory region of the EO gene increased developmental uniformity of silkworm individuals through regulating 20E metabolism, partially explaining transformation of a domestication developmental trait in the domesticated silkworm. Our results emphasize the exceptional role of gene expression regulation in developmental transition of domesticated animals.

Keywords: domestication; ecdysone oxidase; regulatory region; selective sweep; silkworm; transposable element.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxysteroid Dehydrogenases / genetics*
  • 3-Hydroxysteroid Dehydrogenases / metabolism
  • 5' Flanking Region
  • Animals
  • Bombyx / enzymology
  • Bombyx / genetics*
  • DNA Transposable Elements*
  • Ecdysterone / biosynthesis
  • Evolution, Molecular
  • Gene Expression
  • Gene Expression Regulation, Developmental
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Linkage Disequilibrium
  • Mutagenesis, Insertional
  • Regulatory Sequences, Nucleic Acid
  • Sequence Analysis, DNA

Substances

  • DNA Transposable Elements
  • Insect Proteins
  • Ecdysterone
  • 3-Hydroxysteroid Dehydrogenases
  • ecdysone oxidase