The "transition zone" of the cilium-like regions in the Drosophila spermatocytes and the role of the C-tubule in axoneme assembly

Exp Cell Res. 2018 Oct 1;371(1):262-268. doi: 10.1016/j.yexcr.2018.08.020. Epub 2018 Aug 18.

Abstract

The fruit-fly Drosophila melanogaster harbours different types of ciliary structures: ciliary projections associated with neurons of type I and cilium-like regions (CLRs) found during male gametogenesis. The latter deserve particular attention since they are morphologically similar to vertebrate primary cilia and transform into the sperm axonemes during spermiogenesis. Although, all the centrioles are able to organize the CLRs, we found that the mother centriole docks first to the plasma membrane suggesting a new intrinsic functional asymmetry between the parent centrioles. We also show that the CLRs lack the Y-links that connect the axoneme doublets with the plasma membrane in conventional primary cilia. Moreover, the C-tubules, that are lacking in the axoneme of the primary cilia, persisted along the CLRs albeit modified into longitudinal blades. Remarkably, mutant flies in which the CLRs are devoid of the C-tubules or their number is reduced lack sperm axonemes or have incomplete axonemes. Therefore, the C-tubules are dispensable for the assembly of the CLRs but are essential for sperm axoneme elongation and maintenance in Drosophila.

Keywords: C-tubule dynamics; Ciliary structures; Drosophila; Male gametogenesis; Transition zone.

MeSH terms

  • Animals
  • Axoneme / metabolism
  • Axoneme / ultrastructure
  • Cell Cycle Proteins / deficiency
  • Cell Cycle Proteins / genetics
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Centrioles / metabolism
  • Centrioles / ultrastructure*
  • Cilia / metabolism
  • Cilia / ultrastructure*
  • Drosophila Proteins / deficiency
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Drosophila melanogaster / ultrastructure*
  • Gene Expression Regulation, Developmental
  • Male
  • Meiosis
  • Microscopy, Electron, Transmission
  • Mutation
  • Pupa / genetics
  • Pupa / growth & development
  • Pupa / metabolism
  • Pupa / ultrastructure*
  • Spermatocytes / growth & development
  • Spermatocytes / metabolism
  • Spermatocytes / ultrastructure*
  • Spermatogenesis / genetics*

Substances

  • Cell Cycle Proteins
  • Cnb protein, Drosophila
  • Drosophila Proteins
  • UNC protein, Drosophila