Abstract
Oocytes of many invertebrate and vertebrate species contain a characteristic organelle complex known as the Balbiani body (Bb). Until now, three principal functions have been ascribed to this complex: delivery of germ cell determinants and localized RNAs to the vegetal cortex/posterior pole of the oocyte, transport of the mitochondria towards the germ plasm, and participation in the formation of lipid droplets. Here, we present the results of a computer-aided 3D reconstruction of the Bb in the growing oocytes of an insect, Thermobia domestica. Our analyses have shown that, in Thermobia, the central part of each fully developed Bb comprises a single intricate mitochondrial network. This “core” network is surrounded by several isolated bean-shaped mitochondrial units that display lowered membrane potential and clear signs of degeneration. In light of the above results and recent theoretical models of mitochondrial quality control, the role of the Bb is discussed. We suggest that, in addition to the aforementioned functions, the Bb is implicated in the selective elimination of dysfunctional mitochondria during oogenesis.Electronic supplementary materialThe online version of this article (doi:10.1007/s00441-016-2414-x) contains supplementary material, which is available to authorized users.
Highlights
Oocytes of many invertebrate and vertebrate species contain a transient assemblage of organelles known as the Balbiani body (Bb) or mitochondrial cloud
To reconstruct Thermobia 3D organization of the Bb in various developmental stages, we used serial sections of 5 early meiotic and 5 previtellogenic oocytes dissected from two young females
The results presented here clearly indicate that in Thermobia the Bb is not involved in the directional transport of organelles/macromolecules to certain oocyte region(s), and that polarity dictated by the position of this organelle assemblage is transient and lasts only until the beginning of a previtellogenic growth
Summary
Oocytes of many invertebrate and vertebrate species contain a transient assemblage (complex) of organelles known as the Balbiani body (Bb) or mitochondrial cloud. The structure and composition of the Bb differ even between related species and are highly dynamic during subsequent stages of Bb morphogenesis, i.e. its formation, gradual development and ultimate fragmentation (Heasman et al 1984; Cox and Spradling 2003; Marlow and Mullins 2008; reviewed in Kloc et al 2004a) Despite this variability, Bbs always contain two essential elements: numerous tightly clustered mitochondria, and electron-dense granulo-fibrillar material, termed the nuage (composition and functioning of nuage is discussed in Jaglarz et al 2011; Kloc et al 2014). In this context, that the Bb represents an evolutionary ancestral organelle involved in the localization and/or enrichment of maternal macromolecules and organelles in certain oocyte regions (reviewed by Kloc et al 2014)
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