Anterior localization of maternal mRNAs in a short germ insect lacking bicoid

Evol Dev. 2005 Mar-Apr;7(2):142-9. doi: 10.1111/j.1525-142X.2005.05016.x.

Abstract

Anterior morphogens have long been postulated to function in early pattern formation in several insect taxa. Genetic studies in Drosophila revealed that the Bicoid protein performs as such in the fly. Maternally provided bicoid (bcd) mRNA is localized at the anterior pole of the oocyte and, upon fertilization, acts as the source of a morphogenetic gradient of Bicoid protein. Despite its central role in Drosophila, it is believed that bicoid arose rather recently during dipteran evolution through duplication of the Hox3 ortholog zen. Here we show that in the red flour beetle Tribolium castaneum, RNAs of the homologs of the Drosophila transcription factors eagle (Tc'eagle) and pangolin (Tc'pan) are maternally localized at the anterior pole of the egg. It is possible that underlying mechanisms for the anterior localization of maternal RNAs evolved independently in the two clades. However, considering the complexity of the process in Drosophila, it is more tempting to speculate that the molecular machinery evolved only once during insect evolution. Under this assumption, it was present before bicoid evolved as an anterior morphogen. To become concentrated at the anterior pole of the egg bicoid may only have had to acquire a signal sequence that was recognized by the preexisting localization machinery. Although we were not able to demonstrate a function in early embryogenesis for Tc'eagle or Tc'pan, our findings suggest that other factors likely function as anterior determinants in Tribolium, and other nondipteran insects.

Publication types

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

MeSH terms

  • Animals
  • Drosophila Proteins / biosynthesis
  • Drosophila melanogaster
  • Evolution, Molecular
  • Gene Expression Regulation, Developmental / physiology*
  • Homeodomain Proteins
  • Ovum / cytology
  • Ovum / physiology
  • RNA, Messenger / metabolism
  • Receptors, Steroid / biosynthesis
  • Repressor Proteins / biosynthesis
  • Trans-Activators / deficiency*
  • Transcription Factors / biosynthesis
  • Tribolium / cytology
  • Tribolium / embryology*
  • Tribolium / genetics

Substances

  • Drosophila Proteins
  • Homeodomain Proteins
  • RNA, Messenger
  • Receptors, Steroid
  • Repressor Proteins
  • Trans-Activators
  • Transcription Factors
  • bcd protein, Drosophila
  • eg protein, Drosophila
  • pan protein, Drosophila