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Sex chromosomes, synapsis, and cohesins: a complex affair

Abstract

During first meiotic prophase, homologous chromosomes are held together by the synaptonemal complex, a tripartite proteinaceous structure that extends along the entire length of meiotic bivalents. While this feature is applicable for autosomes, sex chromosomes often escape from this rule. Many species present sex chromosomes that differ between them in their morphology, length, and gene content. Moreover, in some species, sex chromosomes appear in a single dose in one of the sexes. In all of these cases, the behavior of sex chromosomes during meiosis is conspicuously affected, and this includes the assembly and dynamics of the synaptonemal complex. We review in this study the structure of the synaptonemal complex in the sex chromosomes of three groups of organisms, namely: mammals, orthopterans, and hemipterans, which present different patterns of sex chromosome structure and behavior. Of special interest is the analysis of the organization of the axial/lateral elements of the synaptonemal complex in relation to other axial structures organized along meiotic chromosomes, mainly the cohesin axis. The differences found in the behavior of both axial structures reveal that while the organization of a cohesin axis along sex chromosomes is a conserved feature in most organisms and it shows very little morphological variations, the axial/lateral elements of the synaptonemal complex present a wide range of structural modifications on these chromosomes.

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Acknowledgements

We are indebt to Dr. Carlos García de la Vega for his helpful comments on the manuscript, and to Dr. Christa Heyting (Wageningen, The Netherlands) and Dr. José Luis Barbero (Madrid, Spain) for providing antibodies. This work was supported by grants BMC2002-00043 and BFU2005-05668-C03-01 from Ministerio de Educación y Ciencia (Spain), grant 1001160016 from Universidad Autónoma de Madrid (Spain), FONDECYT grants 2000008, 1040910, and 7040174 (Chile), and a grant from Centro de Estudios de América Latina-BSCH (Spain). RdlF received support from FGUAM and Olympus Optical España S.A.

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Correspondence to Jesús Page.

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The synaptonemal complex—50 years

Communicated by R. Benavente

Electronic supplementary material

3-D reconstruction of a Locusta migratoria pachytene spermatocyte immunolabelled against the cohesin subunit SMC3 (green). At the right movie the chromatin is counterstained with DAPI (blue). The position of the X chromosome is indicated by an X. Notice the presence of a single and continuous cohesin axis inside the chromatin of the X chromosome, that is thinner than that exhibited by the synapsed autosomal bivalents. For the correct visualization of the movie select the boucle option in the video player (MOV 917 kb)

3-D reconstruction of a Locusta migratoria pachytene spermatocyte immunolabelled against the cohesin subunit SMC3 (green). At the right movie the chromatin is counterstained with DAPI (blue). The position of the X chromosome is indicated by an X. Notice the presence of a single and continuous cohesin axis inside the chromatin of the X chromosome, that is thinner than that exhibited by the synapsed autosomal bivalents. For the correct visualization of the movie select the boucle option in the video player (MOV 917 kb)

3D reconstruction throughout two spermatocyte nuclei of the hemipteran species Graphosoma italicum. In both spermatocytes the chromatin is stained with DAPI (blue) and the sex chromosomes are located at the nuclear periphery (XY). In the left reconstruction the SYCP3 protein of the synaptonemal complex is stained (green), the absence of signalling inside the sex chromatin being evident. Note that the position of the autosomal synaptonemal complexes appears in focal plains that are different from those occupied by the sex chromosomes. On the contrary, in the right reconstruction, in which the SMC3 subunit of the cohesin complex is detected (green), conspicuous threads are located inside the sex chromatin. For the correct visualization of the movie select the boucle option in the video player (MOV 720 kb)

3D reconstruction throughout two spermatocyte nuclei of the hemipteran species Graphosoma italicum. In both spermatocytes the chromatin is stained with DAPI (blue) and the sex chromosomes are located at the nuclear periphery (XY). In the left reconstruction the SYCP3 protein of the synaptonemal complex is stained (green), the absence of signalling inside the sex chromatin being evident. Note that the position of the autosomal synaptonemal complexes appears in focal plains that are different from those occupied by the sex chromosomes. On the contrary, in the right reconstruction, in which the SMC3 subunit of the cohesin complex is detected (green), conspicuous threads are located inside the sex chromatin. For the correct visualization of the movie select the boucle option in the video player (MOV 720 kb)

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Page, J., de la Fuente, R., Gómez, R. et al. Sex chromosomes, synapsis, and cohesins: a complex affair. Chromosoma 115, 250–259 (2006). https://doi.org/10.1007/s00412-006-0059-3

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Keywords

  • Synaptonemal Complex
  • Meiotic Prophase
  • Cohesin Complex
  • Cohesin Subunit
  • Synaptonemal Complex Protein