On the Role of Transcription in Meiosis
- Authors: Saifitdinova A.F.1,2,3
-
Affiliations:
- Herzen State Pedagogical University of Russia
- Saint Petersburg State University
- Institute of Cytology Russian Academy of Science
- Issue: Vol 56, No 5 (2025)
- Pages: 185-195
- Section: ТОЧКА ЗРЕНИЯ
- URL: https://journals.rcsi.science/0475-1450/article/view/378205
- DOI: https://doi.org/10.7868/S3034626625050022
- ID: 378205
Cite item
Abstract
Transcriptional activity in cells has traditionally been viewed solely in the context of protein biogenesis, serving as a step in the expression of genetic information. However, the discovery of diverse non-coding and regulatory RNAs — many of which function in the nucleus — calls for a reevaluation of transcription’sbroader role in cellular processes. In gametogenesis, transcription has primarily been studied in relation to mRNA stockpiling, particularly in species exhibiting hypertranscriptional oogenesis, where lampbrush chromosomes persist in the oocyte nucleus over an extended period. This review reassesses the significance of transcription in meiosis, integrating data on its dynamic regulation during oogenesis and spermatogenesis across different organisms. Special focus is given to evolutionary conserved mechanisms underlying meiotic recombination of chromosomes. Using heteromorphic and unpaired sex chromosomes as a model, weexplore the peculiarities of inheritance of epigenetic information in the absence of meiotic pairing influence. Additionally, wehighlight features of the of the RNA polymerase II complex, which create the necessary conditions for proper alignment and synapsing of homologous chromosomes during meiotic recombination. These insights advance our understanding of transcription as a critical player in ensuring accurate chromosomal segregation and correct reparation of double breaks during meiotic recombination.
About the authors
A. F. Saifitdinova
Herzen State Pedagogical University of Russia; Saint Petersburg State University; Institute of Cytology Russian Academy of Science
Email: saifitdinova@mail.ru
48 Moyka Embankment, 191186 St. Petersburg, Russian Federation; 7/9 Universitetskaya Embankment, 199034 St. Petersburg, Russia; 4 Tikhoretsky prospect, 194064 St. Petersburg, Russian Federation
References
- Bogdanov Yu.F., Grishaeva T.M. Conservatism, variability and evolution. Moscow: Association of Scientific Publications of the KMC, 2020. 345 p. ISBN 978-5-907213-73-9. (In Russ.)
- Bogdanov Yu.F., Kolomiets O.L. Synaptonemic complex—an indicator of meiosis dynamics and chromosome variability. Moscow: Association of Scientific Publications of the CMC, 2007. 358 p. ISBN 978-5-87317-370-9. (In Russ.)
- Gaginskaya E.R. Lamp brush chromosomes from amphibian oocytes. Cytology. 1989. V. 31. No. 11. P. 1267–1291. (In Russ.)
- Saifitdinova A.F., Galkina S.A., Gaginskaya E.R. The evolution of ideas about the biological significance of the phenomenon of lamp brush-type chromosomes. Genetics. 2021. V. 57. No. 5. P. 491–507. (In Russ.) https://doi.org/10.31857/S0016675821050106
- Akhtar M.S., Heidemann M., Tietjen J.R., et al. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Molecular Cell. 2009. V. 34. P. 387–393. https://doi.org/10.1016/j.molcel.2009.04.016
- Angelier N., Bonnanfant-Jais M. L., Moreau N., et al. DNA methylation and RNA transcriptional activity in amphibian lampbrush chromosomes. Chromosoma. 1986. V. 94. P. 169–182. https://doi.org/10.1007/BF00288491
- Bataille A. R., Jeronimo C., Jacques P. E., et al. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Molecular Cell. 2012. V. 45. P. 158–170. https://doi.org/10.1016/j.molcel.2011.11.024
- Celeste A., Fernandez-Capetillo O., Kruhlak M. J., et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biology. 2003. V. 5. P. 675–679. https://doi.org/10.1038/ncb1004.
- Chen Q., Zeng Y., Kang J., et al. Enhancer RNAs in transcriptional regulation: recent insights. Frontiers in Cell and Developmental Biology. 2023. V. 11. No. 1205540. https://doi.org/10.3389/fcell.2023.1205540.
- Chu D. S., Shakes D. C. Spermatogenesis. Advances in Experimental Medicine and Biology. 2013. V. 757. P. 171–203. https://doi.org/10.1007/978-1-4614-4015-4_7.
- Davidson E. H., Hough B. R. Genetic information in oocyte RNA. Journal of Molecular Biology. 1971. V. 56. No. 3. P. 491–506. https://doi.org/10.1016/0022-2836(71)90396-2.
- Deryusheva S., Krasikova A., Kulikova T., et al. Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription analysis on lampbrush chromosomes. Chromosoma. 2007. V. 116. P. 519–530. https://doi.org/10.1007/s00412-007-0117-5
- Efimova O.A., Pendina A.A., Tikhonov A.V., et al. Chromosome hydroxymethylation patterns in human zygotes and cleavage-stage embryos. Reproduction. 2015. V. 149. No. 3. P. 223–233. https://doi.org/10.1530/REP-14-0343
- Egloff S., O'Reilly D., Chapman R.D., et al. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science. 2007. V. 318. P. 1777–1779. https://doi.org/10.1126/science.1145989
- Egloff S., Zaborowska J., Laitem C., et al. Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes. Molecular Cell. 2012. V. 45. P. 111–122. https://doi.org/10.1016/j.molcel.2011.11.006
- Eick D., Geyer M. The RNA polymerase II carboxy-terminal domain (CTD) code. Chemical Reviews. 2013. V. 113.
- Fernandez-Capetillo O., Allis C.D., Nussenzweig A. Phosphorylation of histone H2B at DNA double-strand breaks. Journal of Experimental Medicine. 2004. V. 199. P. 1671–1677. https://doi.org/10.1084/jem.20032247
- Gaginskaya E., Kulikova T., Krasikova A. Avian lampbrush chromosomes: A powerful tool for exploration of genome expression. Cytogenetic and Genome Research. 2009. V. 124. P. 251–267. https://doi.org/10.1159/000218130
- Gall J.G., Murphy C., Callan H.G., et al. Chapter 8 lampbrush chromosomes. Methods in Cell Biology. 1991. V. 36.
- Gall J. G., Murphy C. Assembly of lampbrush chromosomes from sperm chromatin. Molecular Biology of the Cell. 1998. V. 9. P. 733–747. https://doi.org/10.1091/mbc.9.4.733
- Glover-Cutter K., Larochelle S., Erickson B., et al. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Molecular and Cellular Biology. 2009. V. 29. P. 5455–5464. https://doi.org/10.1128/MCB.00637-09
- Gnatt A. L., Cramer P., Fu J., et al. Structural basis of transcription: an RNA polymerase II elongation complex at 3 Å resolution. Science. 2001. V. 292. No. 5523. P. 1876–1882. https://doi.org/10.1126/science.1059495
- Goldstein P., Slaton D.E. The synaptonemal complexes of Caenorhabditis elegans: comparison of wild-type and mutant strains and pachytene karyotype analysis of wild-type. Chromosoma. 1982. V. 84. P. 585–597. https://doi.org/10.1007/BF00292857
- Grummt I. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Progress in nucleic acid research and molecular biology. 1999. V. 62. P. 109–154. https://doi.org/10.1016/s0079-6603(08)60506-1
- Hirose Y., Ohkuma Y. Phosphorylation of the C-terminal domain of RNA polymerase II plays central roles in the integrated events of eucaryotic gene expression. Journal of Biochemistry. 2007. V. 141. P. 601–608. https://doi.org/10.1093/jb/mvm090
- Ho C.K., Shuman S. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Molecular Cell. 1999. V. 3. P. 405–411. https://doi.org/10.1016/S1097-2765(00)80468-2
- Holstege F.C., van der Vliet P.C., Timmers H.T. Opening of an RNA polymerase II promoter occurs in two distinct steps and requires the basal transcription factors IIE and IIH. The EMBO Journal. 1996. V. 15. No. 7. P. 1666–1677.
- Holstege F. C., Fiedler U., Timmers H. T. Three transitions in the RNA polymerase II transcription complex during initiation. The EMBO Journal. 1997. V. 16. № 24. P. 7468–7480. https://doi.org/10.1093/emboj/16.24.7468
- Hurwitz J. The discovery of RNA polymerase. Journal of Biological Chemistry. 2005. V. 280. No. 52. P. 42477–42485. https://doi.org/10.1074/jbc.X500006200
- Kajitania T., Katoc H., Chikashiged Y., et al. Ser7 of RNAPII–CTD facilitates heterochromatin formation by linking ncRNA to RNAi. Proceedings of the National Academy of Sciences of the USA. 2017. V. 114. No. 52. P. E11208–E11217. https://doi.org/10.1073/pnas.1714579115
- Kornberg, R. Eukaryotic transcriptional control. Trends in Cell Biology. 1999. V. 9. No. 12. P. M46–M49. https://doi.org/10.1016/S0962-8924(99)01679-7
- Kota, S. K., Feil, R. Epigenetic transitions in germ cell development and meiosis. Developmental Cell. 2010. V. 19. P. 675–686. https://doi.org/10.1016/j.devcel.2010.10.009
- Kulikova, T., Surkova, A., Zlotina, A., et al. Mapping epigenetic modifications on chicken lampbrush chromosomes.
- Molecular cytogenetics. 2020. V. 13. No. 1. P. 1–15. https://doi.org/10.1186/s13039-020-00496-0
- Li X., Manley J. L. Cotranscriptional processes and their influence on genome stability. Genes & Development. 2006. V. 20. P. 1838–1847. https://doi.org/10.1101/gad.1438306
- Link J., Jantsch V. Meiotic chromosomes in motion: a perspective from Mus musculus and Caenorhabditis elegans. Chromosoma. 2019. V. 128. P. 317–330. https://doi.org/10.1007/s00412-019-00698-5
- Liu G.-L., Gall J. G. Induction of human lampbrush chromosomes. Chromosome Research. 2012. V. 20. P. 971–978. https://doi.org/10.1007/s10577-012-9331-y
- Lu H., Flores O., Weinmann R., et al. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proceedings of the National Academy of Sciences of the USA. 1991. V. 88. No. 22. P. 10004–10008. https://doi.org/10.1073/pnas.88.22.10004
- Maxon M.E., Goodrich J.A., Tjian R. Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: A model for promoter clearance. Genes and Development. 1994. V. 8. No. 5. P. 515–524. https://doi.org/10.1101/gad.8.5.515
- Meinhart A., Cramer P. Recognition of RNA polymerase II carboxy-terminal domain by 3'-RNA-processing factors. Nature. 2004. V. 430. No. 6996. P. 223–226. https://doi.org/10.1038/nature02679
- Mishra K., Kanduri C. Understanding long noncoding RNA and chromatin interactions: what we know so far. NonCoding RNA. 2019. V. 5(4). No. 54. https://doi.org/10.3390/ncrna5040054.
- Monesi V. Synthetic activities during spermatogenesis in the mouse: RNA and protein. Experimental Cell Research. 1965. V. 39. P. 197–224. https://doi.org/10.1016/0014-4827(65)90023-6.
- Nikolov D.B., Chen H., Halay E.D., et al. Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature. 1995. V. 377. P. 119–128. https://doi.org/10.1038/377119a0.
- Nikolov D.B., Burley S.K. RNA polymerase II transcription initiation: a structural view. Proceedings of the National Academy of Sciences of the USA. 1997. V. 94. No. 1. P. 15–22. https://doi.org/10.1073/pnas.94.1.15.
- Orphanides G., Lagrange T., Reinberg D. The general transcription factors of RNA polymerase II. Genes and Development. 1996. V. 10. No. 21. P. 2657–2683. https://doi.org/10.1101/gad.10.21.2657
- Ortega-Recalde O., Day R.C., Gemmell N.J., et al. Zebrafish preserve global germline DNA methylation while sex-linked rDNA is amplified and demethylated during feminization. Nature Communications. 2019. V. 10. No. 3053. https://doi.org/10.1038/s41467-019-10894-7
- Page J., Berríos S., Rufas J.S., et al. The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements. Journal of Cell Science. 2003. V. 116. P. 551–560. https://doi.org/10.1242/jcs.00252
- Page J., de la Fuente R., Manterola M., et al. Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis? Chromosoma. 2012. V. 121. P. 307–326. https://doi.org/10.1007/s00412-012-0364-y
- Parsa J.-Y., Boudoukha S., Burke J., et al. Polymerase pausing induced by sequence-specific RNA-binding protein drives heterochromatin assembly. Genes and Development. 2018. V. 32. P. 953–964. https://doi.org/10.1101/gad.310136.117
- Patel L., Kang R., Rosenberg S. C., et al. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nature Structural & Molecular Biology. 2019. V. 26. P. 164–174. https://doi.org/10.1038/s41594-019-0187-0.
- Rasmussen S. V., Holm P. B. Mechanics of meiosis. Hereditas. 1980. V. 93. P. 187–216. https://doi.org/10.1111/j.1601-5223.1980.tb01360.x.
- Revyakin A., Ebright R. H., Strick T. R. Promoter unwinding and promoter clearance by RNA polymerase: detection by single-molecule DNA nanomanipulation. Proceedings of the National Academy of Sciences of the USA. 2004. V. 101. P. 4776–4780. https://doi.org/10.1073/pnas.0307241101.
- Rothschild G., Zhang W., Lim J., et al. Noncoding RNA transcription alters chromosomal topology to promote isotype-specific class switch recombination. Science Immunology. 2020. V. 5(44), eaay5864. https://www.science.org/doi/10.1126/sciimmunol.aay5864.
- Saifitdinova A., Derjusheva S., Krasikova A., et al. Lampbrush chromosomes of the chaffinch (Fringilla coelebs L.). Chromosome Research. 2003. V. 11. P. 99–113. https://doi.org/10.1023/A:1022859713777
- Sang L., Yang L., Ge Q., et al. Subcellular distribution, localization, and function of noncoding RNAs. Wiley Interdisciplinary Reviews RNA. 2022. V. 13. No. 6: e1729. https://doi.org/10.1002/wrna.e1729. PMID: 35413151
- Schimenti J. Synapsis or silence. Nature Genetics. 2005. V. 37. P. 11–13. https://doi.org/10.1038/ng0105-11
- Shi J., Zhou T., Chen Q. Exploring the expanding universe of small RNAs. Nature Cell Biology. 2022. V. 24. No. 4. P. 415–423. https://doi.org/10.1038/s41556-022-00880-5
- Shinohara A., Ogawa H., Ogawa T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992. V. 69. P. 457–470. https://doi.org/10.1016/0092-8674(92)90447-k
- Shiu P. K., Raju N. B., Zickler D., et al. Meiotic silencing by unpaired DNA. Cell. 2001. V. 107. P. 905–916. https://doi.org/10.1016/s0092-8674(01)00609-2
- Sims R. J. 3rd, Mandal S. S., Reinberg D. Recent highlights of RNA-polymerase-II-mediated transcription. Current Opinion in Cell Biology. 2004. V. 16. No. 3. P. 263–271. https://doi.org/10.1016/j.ceb.2004.04.004
- Sioud M. RNA interference: story and mechanisms. Methods in Molecular Biology. 2021. V. 2282:1–15. https://doi.org/10.1007/978-1-0716-1298-9_1
- Tietjen J. R., Zhang D. W., Rodriguez-Molina J. B., et al. Chemical-genomic dissection of the CTD code. Nature Structural and Molecular Biology. 2010. V. 17. P. 1154–1161. https://doi.org/10.1038/nsmb.1900
- Turner J. M. A. Meiotic sex chromosome inactivation. Development. 2007. V. 134. P. 1823–1831. https://doi.org/10.1242/dev.000018
- Usheva A., Maldonado E., Goldring A., et al. Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein. Cell. 1992. V. 69. No. 5. P. 871–881. https://doi.org/10.1016/0092-8674(92)90297-p
- Viera A., Parra M. T., Arévalo S., et al. X Chromosome Inactivation during grasshopper spermatogenesis. Genes. V. 12(12). Р. 1844. https://doi.org/10.3390/genes12121844
- Willis I. M. RNA polymerase III. Genes, factors and transcriptional specificity. European Journal of Biochemistry. 1993. V. 212. No. 1. P. 1–11. https://doi.org/10.1111/j.1432-1033.1993.tb17626.x
- Zeng, Y., Chen, T. DNA methylation reprogramming during mammalian development. Genes. 2019. V. 10. P. 257. https://doi.org/10.3390/genes10040257. https://doi.org/10.1016/j.fmre.2023.03.006.
Supplementary files


