Mullakhmetov R.I.1, Kondakova E.A.2,3, Maslakov G.P.2,4, Poliushkevich L.O.2, Kulakova M.A.2* 2025. Localization and distribution dynamics of total maternal RNA in oocytes and early embryos of Platynereis dumerilii (Annelida) // Invert. Zool. Vol.22. No.4. P.575–594 [in English].
1 Department of Cytology and Histology, St. Petersburg State University, Universitetskaya Emb., 7/9, St. Petersburg 199034 Russia.
2 Department of Embryology, St. Petersburg State University, Universitetskaya Emb., 7/9, St. Petersburg 199034 Russia.
3 Saint Petersburg Branch of the FSBSI “VNIRO” (“GosNIORKH” named after L.S. Berg), Makarova Emb., 26, St. Petersburg 199053 Russia.
4 Laboratory of Regenerative Biomedicine, Institute of Cytology, Russian Academy of Sciences, Tikhoretskiy Prospekt, 4, St Petersburg 194064 Russia.
* Corresponding author: m.kulakowa@spbu.ru
Roman Mullakhmetov: mullakhmetov.03@mail.ru ORCID https://orcid.org/0009-0007-0700-971X
Ekaterina Kondakova st036262@mail.spbu.ru ORCID https://orcid.org/0000-0002-5117-4858
Georgii Maslakov: ORCID gequris@gmail.com https://orcid.org/0000-0003-0462-7284
Liudmila Poliushkevich: mila.papurika@gmail.com ORCID https://orcid.org/0000-0003-2896-1893
Milana Kulakova: m.kulakowa@spbu.ru ORCID https://orcid.org/0000-0001-9814-3875
doi: 10.15298/invertzool.22.4.05
ABSTRACT: The early developmental events of all multicellular animals are governed by the maternal genome. Maternal RNA plays a crucial role in sustaining the viability and growth of the early embryo, providing molecular instructions for each initial cell division and facilitating the transition to embryonic development under zygotic genome control. Consequently, the fate of each blastomere depends on its unique set of maternal determinants, which may be critically important for the successful progression of stereotypical and invariant cleavage patterns observed in spiralians. How is maternal RNA distributed in the embryo of a typical spiralian representative? What is its quantity, and for how long is it preserved? The laboratory annelid Platynereis dumerilii is an excellent model to address these questions, as it exhibits a highly stereotypical pattern of spiral cleavage and contains at least 4,000 maternally contributed transcripts. However, current transcriptomic approaches have not provided insights into the distribution of maternal RNA among individual blastomeres of P. dumerilii, and single-cell sequencing has yet to be applied to the early developmental stages of this species. To address this critical gap, we quantified the average amount of maternal RNA for a single oocyte and, for the first time, visually characterized its segregation in early P. dumerilii embryos up to the 16-cell stage, prior to zygotic genome activation. Our findings reveal that maternal RNA in P. dumerilii is initially distributed around the oocyte nucleus and rapidly relocates to the animal pole following fertilization. Its subsequent segregation closely aligns with unequal-cleavage dynamics. One cell cycle prior to the first wave of zygotic transcription, nearly all maternal RNA concentrates in the first quartet of micromeres 1a1-1d1 and the first somatoblast 2d. Notably, these localization dynamics diverge from observations in another annelid, Chaetopterus. Our findings offer a foundation for future comparative and experimental studies on how maternal components regulate early development in spiralians.
KEY WORDS: Maternal RNA, oocytes, spiral cleavage, RNA segregation, Platynereis, annelids, nuclear F-actin.
Download PDF, Suppl. files