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

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.

Balbiani body of basal insects is potentially involved in multiplication and selective elimination of mitochondria

“…1 B1). Such organization of early meiotic Bb is characteristic of other basally branched insects 3 , 14 , 27 .…”

“…Interestingly, recent studies showed that the mitochondria constituting the Bb are interconnected forming extensive mitochondrial network that display distinctly higher inner membrane potential than mitochondria in the remaining part of the oocyte cytoplasm (ooplasm) 27 – 29 . The same studies also showed that the ooplasm surrounding the Bb often contains degenerating mitochondria 14 , 27 , 30 . Interpretation of these findings have led to the suggestion that the Bb may participate not only in the transfer of mitochondria to the next generation but also in the selective elimination of defective (containing mutated mtDNA) mitochondrial units 27 , 30 – 34 .…”

“…These proteins, referred to as amyloid-forming proteins, form networks with amyloid-like properties that are capable of recruiting mitochondria and RNA molecules to the nascent Bb 10 , 13 . Currently, it is not known whether similar processes are also involved in the formation of the Bb in invertebrates 14 .…”

“…A common bush-cricket, Meconema meridionale, served as a model in these studies. We selected this species because of the following reasons: (1) the Bb of Meconema , as these of other bush crickets 3 , 14 , is relatively large and easily recognizable, even at the level of light microscopy; (2) oocytes of bush crickets are morphologically simple and devoid of any specialized ooplasm regions, such as the germ/pole plasm 3 , 14 . The latter trait facilitates the analysis of the Bb morphogenesis and (especially) the fate of the Bb constituents after the dispersion of this organelle assemblage.…”

Comparison of Ovarian Morphology and Follicular Disturbances between Two Inbred Strains of Cotton Rats (Sigmodon hispidus)

“…It is still not known how the structural and molecular components of Bbs are assembled into such morphologically intricate complexes. The most important function of mitochondria is to supply cells with metabolic energy (ATP) generated by oxidative phosphorylation [54]. Therefore, we hypothesize that the presence of more MCs might have contributed to more oocytes in the HIS/Hiph strain than in the HIS/Mz strain by maintaining oocyte reserves.…”