Abstract
The synaptonemal complex (SC), a key structure of meiosis that assembles during prophase I, has been initially described 60 years ago. Since then, the structure has been described in many sexually reproducing organisms. However, the SC protein components were characterized in only few model organisms. Surprisingly, they lacked an apparent evolutionary relationship despite the conserved structural organization of the SC. For better understanding of this obvious discrepancy, the evolutionary history of the SC and its individual components has been investigated in Metazoa in detail. The results are consistent with the notion of a single origin of the metazoan SC and provide evidence for a dynamic evolutionary history of the SC components. In this mini review, we recapitulate and discuss new insights into metazoan SC evolution.



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References
Alsheimer M, Baier A, Schramm S, Schütz W, Benavente R (2010) Synaptonemal complex protein SYCP3 exists in two isoforms showing different conservation in mammalian evolution. Cytogenet Genome Res 128:162–168
Baier A, Alsheimer M, Volff JN, Benavente R (2007) Synaptonemal complex protein SYCP3 of the rat: evolutionarily conserved domains and the assembly of higher order structures. Sex Dev 1:161–168
Benavente R, Krohne G, Stick R, Franke WW (1984) Electron microscopic immunolocalization of a karyoskeletal protein of molecular weight 145 000 in nucleoli and perinucleolar bodies of Xenopus laevis. Exp Cell Res 151:224–235
Bolcun-Filas E, Schimenti JC (2012) Genetics of meiosis and recombination in mice. Int Rev Cell Mol Biol 298:179–227
Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, de Rooij DG, Cooke HJ (2007) SYCP2 is required for synaptonemal complex assembly, DSB repair and homologous recombination. J Cell Biol 176:741–747
Bolcun-Filas E, Hall E, Speed R, Taggart M, Grey C, de Massy B, Benavente R, Cooke HJ (2009) Mutation of the mouse Syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLoS Genet 5:e1000393
Bomblies K, Higgins JD, Yant L (2015) Meiosis evolves: adaptation to external and internal environments. New Phytol 208:306–323
Calenda A, Allenet B, Escalier D, Bach JF, Garchon HJ (1994) The meiosis-specific Xmr gene product is homologous to the lymphocyte Xlr protein and is a component of the XY body. EMBO J 13:100–109
Casey AE, Daish TJ, Grutzner F (2015) Identification and characterization of synaptonemal complex genes in monotremes. Gene 567:146–153
Cocquet J, Ellis PJ, Yamauchi Y, Mahadevaiah SK, Affara NA, Ward MA, Burgoyne PS (2009) The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol 7:e1000244
Cole F, Keeney S, Jasin M (2010) Evolutionary conservation of meiotic DSB proteins: more than just Spo11. Genes Dev 24:1201–1207
Costa Y, Cooke HJ (2007) Dissecting the mammalian synaptonemal complex using targeted mutations. Chromosom Res 15:579–589
Costa Y, Speed R, Öllinger R, Alsheimer M, Semple CA, Gautier P, Maratou K, Novak I, Höög C, Benavente R, Cooke HJ (2005) Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J Cell Sci 118:2755–2762
Davies OR, Maman JD, Pellegrini L (2012) Structural analysis of the human SYCE2–TEX12 complex provides molecular insights into synaptonemal complex assembly. Open Biol 2:120099
Franke WW, Kleinschmidt JA, Spring H, Krohne G, Grund C, Trendelenburg MF, Stoehr M, Scheer U (1981) A nucleolar skeleton of protein filaments demonstrated in amplified nucleoli of Xenopus laevis. J Cell Biol 90:289–299
Fraune J, Schramm S, Alsheimer M, Benavente R (2012a) The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination. Exp Cell Res 318:1340–1346
Fraune J, Alsheimer M, Volff JN, Busch K, Fraune S, Bosch TC, Benavente R (2012b) Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans. Proc Natl Acad Sci U S A 109:16588–16593
Fraune J, Brochier-Armanet C, Alsheimer M, Benavente R (2013) Phylogenies of central element proteins reveal the dynamic evolutionary history of the mammalian synaptonemal complex: ancient and recent components. Genetics 195:781–793
Fraune J, Alsheimer M, Redolfi J, Brochier-Armanet C, Benavente R (2014a) Protein SYCP2 is an ancient component of the metazoan synaptonemal complex. Cytogenet Genome Res 144:299–305
Fraune J, Wiesner M, Benavente R (2014b) The synaptonemal complex of the basal metazoan Hydra: more similarities to vertebrate than invertebrate meiosis model organisms. J Genet Genom 41:107–115
Garchon HJ, Loh E, Ho WY, Amar L, Avner P, Davis MM (1989) The XLR sequence family: dispersion on the X and Y chromosomes of a large set of closely related sequences, most of which are pseudogenes. Nucleic Acids Res 17:9871–9888
Gillies CB (1975) Synaptonemal complex and chromosome structure. Annu Rev Genet 9:91–109
Grishaeva TM, Bogdanov YF (2014) Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes. Int J Evol Biol 2014:856230
Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, Höög C (2006) Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 119:4025–4032
Hamer G, Wang H, Bolcun-Filas E, Cooke HJ, Benavente R, Höög C (2008) Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J Cell Sci 121:2445–2451
Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11:124–136
Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291
Kneissel S, Franke WW, Gall JG, Heid H, Reidenbach S et al (2001) A novel karyoskeletal protein: characterization of protein NO145, the major component of nucleolar cortical skeleton in Xenopus oocytes. Mol Biol Cell 12:3904–3918
Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14:1137–1146
Liu JG, Yuan L, Brundell E, Björkroth B, Daneholt B, Höög C (1996) Localization of the N-terminus of SCP1 to the central element of the synaptonemal complex and evidence for direct interactions between the N-termini of SCP1 molecules organized head-to-head. Exp Cell Res 226:11–19
Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11:5091–5100
Offenberg HH, Schalk JA, Meuwissen RL, van Aalderen M, Kester HA, Dietrich AJ, Heyting C (1998) SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res 26:2572–2579
Öllinger R, Alsheimer M, Benavente R (2005) Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell 16:212–217
Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558
Reynard LN, Cocquet J, Burgoyne PS (2009) The multi-copy mouse gene Sycp3-like Y-linked (Sly) encodes an abundant spermatid protein that interacts with a histone acetyltransferase and an acrosomal protein. Biol Reprod 81:250–257
Schmekel K, Meuwissen RL, Dietrich AJ, Vink AC, van Marle J, van Veen H, Heyting C (1996) Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res 226:20–30
Schramm S, Fraune J, Naumann R, Hernandez-Hernandez A, Höög C, Cooke HJ, Alsheimer M, Benavente R (2011) A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet 7:e1002088
Schücker K, Holm T, Franke C, Sauer M, Benavente R (2015) Elucidation of synaptonemal complex organization by super-resolution imaging and isotropic resolution. Proc Natl Acad Sci U S A 112:2029–2033
Shi YQ, Zhuang XJ, Xu B, Hua J, Liao SY, Shi Q, Cooke HJ, Han C (2013) SYCP3-like X-linked 2 is expressed in meiotic germ cells and interacts with synaptonemal complex central element protein 2 and histone acetyltransferase TIP60. Gene 527:352–359
Syrjänen JL, Pellegrini L, Davies OR (2014) A molecular model for the role of SYCP3 in meiotic chromosome organization. eLife 3:e02963
Tarsounas M, Pearlman RE, Gasser PJ, Park MS, Moens PB (1997) Protein-protein interactions in the synaptonemal complex. Mol Biol Cell 8:1405–1414
Touré A, Clemente EJ, Ellis P, Mahadevaiah SK, Ojarikre OA, Ball PA, Reynard L, Loveland KL, Burgoyne PS, Affara NA (2005) Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol 6:R102
Villeneuve AM, Keeney S, Jasin M (2001) Whence meiosis? Cell 106:647–650
von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18:331–411
Wilkins AS, Holliday R (2009) The evolution of meiosis from mitosis. Genetics 181:3–12
Yuan L, Pelttari J, Brundell E, Björkroth B, Zhao J, Liu JG, Brismar H, Daneholt B, Höög C (1998) The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J Cell Biol 142:331–339
Zhou J, Stein P, Leu NA, Chmatal L, Xue J et al (2015) Accelerated reproductive aging in females lacking a novel centromere protein SYCP2L. Hum Mol Genet 24:6505–6514
Acknowledgments
We thank Markus Sauer (Biocenter, Würzburg) for the generous support with super-resolution imaging and Nicola Jones (Biocenter, Würzburg) for the critical reading of the manuscript.
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R.B. is supported by DFG grant Be1168/8-1. C.B.A. is a member of the Institut Universitaire de France (University French Institute).
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The authors declare that they have no competing interests.
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This article is related to the 21st International Chromosome Conference (Foz do Iguaçu, Brazil, July 10–13, 2016).
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Fraune, J., Brochier-Armanet, C., Alsheimer, M. et al. Evolutionary history of the mammalian synaptonemal complex. Chromosoma 125, 355–360 (2016). https://doi.org/10.1007/s00412-016-0583-8
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DOI: https://doi.org/10.1007/s00412-016-0583-8