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Synaptonemal Complex Proteins: Unicity or Universality?

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Abstract

The preparatory pairing of homologous chromosomes is the obligatory step of meiosis. It occurs through formation of synaptonemal complexes (SC): the protein axes of two chromosomes are connected with the help of additional “central space proteins.” These proteins are sometimes species-specific and serve as the object of comparative studies. With the help of bioinformatics methods, we studied proteins structuring the SC central space in animals and fungi. We established that Ecm11 and Gmc2 had a low level of conservation even within the taxon of Ascomycetes. The SIX6OS1 protein of the mouse, as well as SYCE1–SYCE3 and TEX12 in animals, was moderately conserved only within the subphylum of vertebrates, despite these proteins (with the exception of SYCE3) occurring in invertebrates too. Thus, we have confirmed the thesis that, in addition to the common set of meiotic proteins, every evolutionary line of Eukaryotes has developed its own proteins for the formation of SC, the general structure of which is common between all eukaryotes.

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REFERENCES

  1. Page, S.L. and Hawley, R.S., The genetics and molecular biology of the synaptonemal complex, Annu. Rev. Cell Dev. Biol., 2004, vol. 20, pp. 525—558. https://doi.org/10.1146/annurev.cellbio.19.111301.155141

    Article  CAS  PubMed  Google Scholar 

  2. Gao, J. and Colaiácovo, M.P., Zipping and unzipping: protein modifications regulating synaptonemal complex dynamics, Trends Genet., 2018, vol. 34, pp. 232—245. https://doi.org/10.1016/j.tig.2017.12.001

    Article  CAS  PubMed  Google Scholar 

  3. Zickler, D. and Kleckner, N., Meiotic chromosomes: integrating structure and function, Ann. Rev. Genet., 1999, vol. 33, pp. 603—754. https://doi.org/10.1146/annurev.genet.33.1.603

    Article  CAS  PubMed  Google Scholar 

  4. Moses, M.J., Chromosomal structures in crayfish spermatocytes, J. Biophys. Biochem. Cytol.,1956, vol. 2, pp. 215—219. https://doi.org/10.1083/jcb.2.2.215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cahoon, C.K. and Hawley, R.S., Regulating the construction and demolition of the synaptonemal complex, Nat. Struct. Mol. Biol., 2016, vol. 23, pp. 369—377. https://doi.org/10.1038/nsmb.3208

    Article  CAS  PubMed  Google Scholar 

  6. Schmekel, K. and Daneholt, B., The central region of the synaptonemal complex revealed in three dimensions, Trends Cell Biol., 1995, vol. 5, pp. 239—242. https://doi.org/10.1016/s0962-8924(00)89017-0

    Article  CAS  PubMed  Google Scholar 

  7. Hawley, R.S., Solving a meiotic LEGO puzzle: transverse filaments and the assembly of the synaptonemal complex in Caenorhabditis elegans, Genetics, 2011, vol. 189, pp. 405—409. https://doi.org/10.1534/genetics.111.134197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Collins, K.A., Unruh, J.R., Slaughter, B.D., et al., Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila, Genetics, 2014, vol. 198, pp. 219—228. https://doi.org/10.1534/genetics.114.165290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Costa, Y., Speed, R., Ollinger, R., et al., Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis, J. Cell Sci., 2005, vol. 118, pp. 2755—2762. https://doi.org/10.1242/jcs.02402

    Article  CAS  PubMed  Google Scholar 

  10. Hamer, G., Gell, K., Kouznetsova, A., et al., Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex, J. Cell Sci., 2006, vol. 119, pp. 4025—4032. https://doi.org/10.1242/jcs.03182

    Article  CAS  PubMed  Google Scholar 

  11. Schramm, S., Fraune, J., Naumann, R., et al., A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility, PLoS Genet., 2011, vol. 7. e1002088. https://doi.org/10.1371/journal.pgen.1002088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gόmez,-H. L., Felipe-Medina, N., Sáchez-Marti, M., et al., C14ORF39/SIX6OS1 is a constituent of the synaptonemal complex and is essential for mouse fertility, Nat. Commun., 2016, vol. 7, article number 13298. https://doi.org/10.1038/ncomms13298

    Article  CAS  Google Scholar 

  13. Humphryes, N., Leung, W.-K., Argunhan, B., et al., The Ecm11–Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast, PLoS Genet., 2013, vol. 9. e1003194. https://doi.org/10.1371/journal.pgen.1003194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Voelkel-Meiman, K., Cheng, S.-Y., Morehouse, S.J., and MacQueen, A.J., Synaptonemal complex proteins of budding yeast define reciprocal roles in MutSγ-mediated crossover formation, Genetics, 2016, vol. 203, pp. 1091—1103. https://doi.org/10.1534/genetics.115.182923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fraune, J., Schramm, S., Alsheimer, M., and Benavente, R., The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination, Exp. Cell Res., 2012, vol. 318, pp. 1340—1346. https://doi.org/10.1016/j.yexcr.2012.02.018

    Article  CAS  PubMed  Google Scholar 

  16. Bogdanov, Y.F., Grishaeva, T.M., and Dadashev, S.Y., Similarity of the domain structure of proteins as a basis for the conservation of meiosis, Int. Rev. Cytol., 2007, vol. 257, pp. 83—142. https://doi.org/10.1016/S0074-7696(07)57003-8

    Article  CAS  PubMed  Google Scholar 

  17. Grishaeva, T.M. and Bogdanov, Y.F., Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes, Int. J. Evol. Biol., 2014, vol. 2014, article number 856230. https://doi.org/10.1155/2014/856230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Fraune, J., Brochier-Armanet, C., Alsheimer, M., and Benavente, R., Phylogenies of central element proteins reveal the dynamic evolutionary history of the mammalian synaptonemal complex: ancient and recent components, Genetics, 2013, vol. 195, pp. 781—793. https://doi.org/10.1534/genetics.113.156679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fraune, J., Brochier-Armanet, C., Alsheimer, M., et al., Evolutionary history of the mammalian synaptonemal complex, Chromosoma, 2016, vol. 125, pp. 355—360. https://doi.org/10.1007/s00412-016-0583-8

    Article  PubMed  Google Scholar 

  20. Ramesh, M.A., Malik, S.-B., and Logsdon, J.M., Jr., A phylogenomic inventory of meiotic genes: evidence for sex in giardia and an early eukaryotic origin of meiosis, Curr. Biol., 2005, vol. 15, pp. 185—191. https://doi.org/10.1016/j.cub.2005.01.003

    Article  CAS  PubMed  Google Scholar 

  21. Bogdanov, Y.F. and Grishaeva, T.M., Konservatizm, izmenchivost’ i evolyutsiya meioza (Conservatism, Variation and Evolution of Meiosis), Moscow: KMK, 2020, pp. 231—245, 260—277.

  22. Westergaard, M. and von Wettstein, D., The synaptonemal complex, Ann. Rev. Genet., 1972, vol. 6, pp. 71—110. https://doi.org/10.1146/annurev.ge.06.120172.000443

    Article  CAS  PubMed  Google Scholar 

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Funding

The study was supported by the Russian Foundation for Basic Research, project no. 17-00-00430 (17-00-00429 KOMFI), and by the state assignment of the Vavilov Institute of General Genetics, Russian Academy of Sciences, topic no. 0112-2019-0002.

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  1. Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991, Moscow, Russia

    T. M. Grishaeva & Yu. F. Bogdanov

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  1. T. M. Grishaeva
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  2. Yu. F. Bogdanov
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Correspondence to T. M. Grishaeva.

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The authors declare they have no conflict of interest.

The present study does not contain any research using animals as subjects.

The present study does not contain any research involving people as subjects.

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Translated by A. Lisenkova

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Grishaeva, T.M., Bogdanov, Y.F. Synaptonemal Complex Proteins: Unicity or Universality?. Russ J Genet 57, 912–919 (2021). https://doi.org/10.1134/S1022795421080068

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