Comparison of RNA localization during oogenesis within Acipenser ruthenus and Xenopus laevis

Abstract

The oocyte is a unique cell, from which develops a complex organism comprising of germ layers, tissues and organs. In some vertebrate species it is known that the asymmetrical localization of biomolecules within the oocyte is what drives the spatial differentiation of the daughter cells required for embryogenesis. This asymmetry is first established to produce an animal-vegetal (A-V) axis which reflects the future specification of the ectoderm, mesoderm, and endoderm layers. Several pathways for localization of vegetal maternal transcripts have already been described using a few animal models. However, there is limited information about transcripts that are localized to the animal pole, even though there is accumulating evidence indicating its active establishment. Here, we performed comparative TOMO-Seq analysis on two holoblastic cleavage models: Xenopus laevis and Acipenser ruthenus oocytes during oogenesis. We found that there were many transcripts that have a temporal preference for the establishment of localization. In both models, we observed vegetal transcript gradients that were established during either the early or late oogenesis stages and transcripts that started their localization during the early stages but became more pronounced during the later stages. We found that some animal gradients were already established during the early stages, however the majority were formed during the later stages of oogenesis. Some of these temporally localized transcripts were conserved between the models, while others were species specific. Additionally, temporal de novo transcription and also degradation of transcripts within the oocyte were observed, pointing to an active remodeling of the maternal RNA pool.

Asymmetry in previtellogenic and early vitellogenic oocytes, ultrastructure of follicular cells and egg envelope in the pigmented sterlet, Acipenser ruthenus L. 1758 (Chondrostei, Acipenseriformes)

“…Recently, a continuous increase in the asymmetrical localization of transcripts (mRNAs) grip2, exd2, cnot11, uhrf1, dnd1, arhgef18, prss23 , and crk in the ooplasm of early and advanced vitellogenic oocytes of A. ruthenus was described (Iegorova et al, 2022). The asymmetry is established during the early (vegetally localized grip2 mRNA) or advanced stage (vegetally localized cnot11, dnd1 mRNAs) and involves their temporal de novo transcription and degradation.…”

“…Recently, a continuous increase in the asymmetrical localization of transcripts (mRNAs) grip2, exd2, cnot11, uhrf1, dnd1, arhgef18, prss23, and crk in the ooplasm of early and advanced vitellogenic oocytes of A. ruthenus was described (Iegorova et al, 2022). The In the animal region, the so-called polar transcripts are preferentially located (crk mRNA).…”

“…Although the spatial organization of vitellogenic oocytes was described in A. baerii , in A. gueldenstaedtii (Dettlaff et al, 1993; Le Menn & Pelissero, 1991; Le Menn et al, 2018; Żelazowska & Fopp‐Bayat, 2017a; Żelazowska, 2010, 2014), and recently in A. ruthenus (Iegorova et al, 2022), this phase is not fully explained. In these species, the nucleus is displaced slowly to the animal region in the oocyte, the granular and homogeneous ooplasms are no longer recognizable and the yolk is accumulated (Iegorova et al, 2022; Le Menn & Pelissero, 1991; Le Menn et al, 2018; Żelazowska & Fopp‐Bayat, 2017a). Three regions are distinguished in the ooplasm: the perinuclear, the endoplasm, and the periplasm (Iegorova et al, 2022; Żelazowska, 2014; Żelazowska & Fopp‐Bayat, 2017a).…”

“…In these species, the nucleus is displaced slowly to the animal region in the oocyte, the granular and homogeneous ooplasms are no longer recognizable and the yolk is accumulated (Iegorova et al, 2022; Le Menn & Pelissero, 1991; Le Menn et al, 2018; Żelazowska & Fopp‐Bayat, 2017a). Three regions are distinguished in the ooplasm: the perinuclear, the endoplasm, and the periplasm (Iegorova et al, 2022; Żelazowska, 2014; Żelazowska & Fopp‐Bayat, 2017a). The egg envelope is deposited on the surface of the oocyte and is perforated by numerous radial canals formed around the microvilli of the oocyte and processes of FCs ( zona radiata ) (Le Menn & Pelissero, 1991; Le Menn et al, 2018; Żelazowska, 2010, 2014; Żelazowska & Fopp‐Bayat, 2017a).…”

Application of spatial transcriptome technologies to neurological diseases

“…Tomo-Seq can be used for whole organisms as well as isolated organs or tissues (Kruse et al, 2016;Naraine et al, 2022), and its detection throughput is large enough to reconstruct the spatial gene expression of thousands of genes. It is an unbiased and systematic way to describe the development of animals, appropriate for developmental biology studies (Boogerd et al, 2022;Iegorova et al, 2022). However, it has the limitation of not providing the spatial resolution of microscopy-based techniques.…”