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Cohesin axis maturation and presence of RAD51 during first meiotic prophase in a true bug

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Abstract

We have analyzed in a true bug, Graphosoma italicum (Pentatomidae, Hemiptera), the temporal and functional relationships between recombination events, synapsis progression, and SMC1α and SMC3 cohesin axis maturation throughout the male first meiotic prophase. The localization of the histone variant histone H3 trimethylated at lysine 9 at chromosome ends has allowed us to determine the association of these heterochromatic domains through prophase I stages. Results highlighted that cohesins provide to be good markers for synapsis progression since the formation, morphology, and development of the SMC1α and SMC3 cohesin axes resemble the synaptonemal complex dynamics and, also, that in this species the initiation of recombination precedes synapsis. In addition, we have carried out an accurate cytological characterization of the diffuse stage, which takes place after pachytene, and also analyzed the presence of the cohesin subunits, SMC1α and SMC3, and the recombinase RAD51 at this stage. The mechanisms underlying the absence of SMC1α and SMC3 axes from the diffuse stage onwards are discussed.

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Acknowledgements

We would like to express our gratitude to Consejería de Medio Ambiente y Ordenación del Territorio (Comunidad de Madrid; España) for emitting the authorization for animal recollections in natural populations, to Dr. José Luis Barbero for generously supplying us the anti-SMC3 anti-SMC1α antibodies, to Dr. Kim McKim for his generous gift of the anti-H2Av antibody, and to Dr. García de la Verga for the critical reading of the manuscript. This work was supported by grants BFU2006-06655, BFU2005-02431, BFU200800459, and BFU2008-00300-BCM from the Ministerio de Educación y Ciencia Spain.

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Authors and Affiliations

  1. Departamento de Biología, Edificio de Biológicas, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    Alberto Viera, María Teresa Parra, Adela Calvente, Rocío Gómez, Roberto de la Fuente, José Ángel Suja, Jesús Page & Julio S. Rufas

  2. Departamento de Genética, Facultad de Biología, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Juan Luis Santos

  3. Unidad de Biología Celular, Departamento de Biología, Facultad de Ciencias, Edificio de Ciencias Biológicas, Universidad Autónoma de Madrid, C/Darwin 2, 28049, Madrid, Spain

    Julio S. Rufas

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  1. Alberto Viera
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Correspondence to Julio S. Rufas.

Additional information

Communicated by T. Orr-Weaver

Note added in proofs

A special issue dedicated exclusively to SMC proteins has recently been published in the journal Chromosome Research (vol. 17, 2009). No references about these reviews are included in the text.

Electronic supplementary material

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SMC3 distribution in squashed spermatocytes. 3-D reconstruction of a field of spermatocytes immunolabeled for SMC3 (green) and DAPI-stained (pseudocolored in red). Leptotene (Le), zygotene (Zy), early-, mid-, and late-pachytene (Pearly, Pmid, and Plate), diffuse, and metaphase I (MI) spermatocytes are observed and one spermatid (Sp). Note the presence of a brighter structure in pachytene and diffuse spermatocytes, corresponding to the chromatin of the sex chromosomes (XY). This video corresponds to the reconstructions of the spermatocytes shown in Fig. 1. See text for further details (MOV 710 kb)

Video 2

RAD51 distribution in a pachytene spermatocyte. 3-D reconstruction of a squashed pachytene spermatocyte immunolabeled for RAD51 (red) and DAPI-stained (blue). Despite RAD51 being located on the autosomal chromatin, it is noteworthy that sex chromosomes (XY) do not show RAD51 signals (MOV 3250 kb)

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Viera, A., Santos, J.L., Parra, M.T. et al. Cohesin axis maturation and presence of RAD51 during first meiotic prophase in a true bug. Chromosoma 118, 575–589 (2009). https://doi.org/10.1007/s00412-009-0218-4

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