Meiosis, Balbiani body and early asymmetry of Thermobia oocyte

Abstract

The meiotic division guarantees maintenance of a genetic diversity; it consists of several stages, with prophase I being the longest and the most complex. We decided to follow the course of initial stages of meiotic division in ovaries of Thermobia domestica using modified techniques of squash preparations, semithin sections, and electron microscopy. We show that germaria contain numerous germline cells that can be classified into three categories: cystoblasts, meiotic oocytes, and growing previtellogenic oocytes. The cystoblasts are located most apically. The meiotic oocytes occupy the middle part of the germarium, and the previtellogenic oocytes can be found in the most basal part, near the vitellarium. Analyses of the semithin sections and squash preparations show that post leptotene meiotic chromosomes gather in one region of the nucleoplasm where they form the so-called bouquet. The telomeres of the bouquet chromosomes are attached to a relatively small area (segment) of the nuclear envelope. Next to this envelope segment, the nucleolar organizers are also located. We show that in concert to sequential changes inside the oocyte nuclei, rearrangement of organelles within the ooplasm (oocyte cytoplasm) takes place. This leads to the formation of the Balbiani body and consequent asymmetry of the ooplasm. These early nuclear and cytoplasmic asymmetries, however, are transient. During diplotene, the chromosome bouquet disappears, while the Balbiani body gradually disperses throughout the ooplasm. Finally, our observations indicate the presence of lampbrush chromosomes in the nuclei of previtellogenic oocytes. In the close vicinity to lampbrush chromosomes, characteristic spherical nuclear bodies are present.

Ovarian nests in cultured females of the Siberian sturgeon Acipenser baerii (Chondrostei, Acipenseriformes)

“…Contrary to meroistic, in the so‐called panoistic insect ovaries all cystoblasts and cystocytes differentiate into the oocytes, except these that undergo degeneration. Development of these oocytes is supported by somatic follicular cells only (Biliński, ; Büning, ; Tworzydło, Marek, Kisiel, & Bilinski, ). In the frog Xenopus laevis in 16‐cell cysts all cystocytes are the pro‐oocytes (Kloc et al, ).…”

“…The early asymmetry of cytoplasm in A. baerii is established in cystocytes during previous stages (leptotene and zygotene) and most probably depends on an interaction between a bouquet of meiotic chromosomes in the nucleoplasm and the precursor of granular ooplasm. In X. laevis , in M. musculus , in D. rerio and in the insect Thermobia domestica , a bouquet of chromosomes formed during the leptotene stage attaches by means of clustered telomeres to the inner nuclear membrane at a side that faces the Balbiani body in the ooplasm (Elkouby et al, ; Kloc et al, ; Lei & Spradling, ; Tworzydło et al, ). The Balbiani body always organizes around centrioles that face intercellular bridges between cystocytes (Kloc et al, ).…”

Coordination of cellular differentiation, polarity, mitosis and meiosis – New findings from early vertebrate oogenesis

“…4B) (Tworzydlo et al, 2016b). Interestingly, Thermobia ovarioles show a more “vertebrate”-like mode of oogenesis, where all germ cells in the germarium are fated to become oocytes, as opposed to some becoming nurse cells like in Drosophila (Tworzydlo et al, 2016b). …”

Selection of mitochondria in female germline cells: is Balbiani body implicated in this process?

“…In some arthropods, e.g., spiders and myriapods, the Bbs are large, conspicuous, and persist in the ooplasm until the advanced stages of oogenesis [ 30 – 34 ]; in other species, the Bbs are relatively small and transient [ 35 – 37 ]. The most detailed and comprehensive description of the Bb morphology and morphogenesis in non-model invertebrates comes from the ultrastructural (EM) analyses of Thermobia domestica (firebrat) oocytes [ 9 , 21 , 37 , 38 ]. This species has been selected as a “model” in our laboratory because of three reasons: T. domestica belongs to the basal insect clade Zygentoma (silverfish), which suggests that in this species, ancestral mechanisms can operate during formation and dispersion of the Bb; The Bb of this species is relatively small and consists of limited number of organelles that obviously simplifies analyses, especially at an EM level; The oocytes and eggs of T. domestica are roughly spherical and do not comprise of any specialized region, e.g., the germ plasm, implying that the Bb in this basal insect is not involved in directional localization of mRNAs and/or organelles to certain oocyte region as it is in model species (frog or fish).…”