Morphogenesis of the Balbiani body in developing oocytes of an orthopteran, Metrioptera brachyptera, and multiplication of female germline mitochondria

J Morphol. 2020 Sep;281(9):1142-1151. doi: 10.1002/jmor.21242. Epub 2020 Aug 7.

Abstract

Balbiani body (Bb) is a female germline specific organelle complex. Although the morphology and morphogenesis of the Bb have been analyzed in numerous vertebrate and invertebrate species, the role and ultimate fate of this organelle assemblage are still under debate. As a result, various functions have been attributed to the Bb in given animal lineages or even species. Our analyses showed that in the bush cricket, Metrioptera brachyptera, the Bb is an elaborate and highly dynamic structure positioned at one side of the oocyte nucleus. It forms in early previtellogenic oocytes and consists of two compartments: perinuclear and cytoplasmic. In the cytoplasmic compartment, characteristic complexes of nuage and polymorphous mitochondria are present. Computer-aided 3D reconstructions revealed that mitochondria clustered around neighboring nuage accumulations remain in a physical contact and form an extensive, though dispersed network. As oogenesis progresses, nuage/mitochondria complexes are partitioned into progressively smaller entities that become separated from each other. Concurrently, the mitochondrial network splits into small individual mitochondria populating the whole ooplasm. Immunohistochemical analysis showed that the latter process involves dynamin-related protein 1 (Drp1). Collectively, our findings suggest that in basal insect species, the Bb might be responsible for the selection as well as multiplication of the oocyte mitochondria.

Keywords: Drp1; mitochondrial network; mitophagy; nuage; oogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromosomal Puffs / physiology*
  • Female
  • Germ Cells / metabolism*
  • Imaging, Three-Dimensional
  • Immunohistochemistry
  • Insecta / anatomy & histology*
  • Mitochondria / metabolism*
  • Mitochondria / ultrastructure
  • Morphogenesis*
  • Oocytes / cytology
  • Oocytes / ultrastructure
  • Ovary / anatomy & histology
  • Vitellogenesis