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First published online June 23, 2005
doi: 10.1242/10.1242/jcs.02391


Journal of Cell Science 118, 2957-2963 (2005)
Published by The Company of Biologists 2005
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Research Article

DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis

Adela Calvente1,*, Alberto Viera1,*, Jesús Page1, M. Teresa Parra1, Rocío Gómez1, José A. Suja1, Julio S. Rufas1,{ddagger} and Juan L. Santos2

1 Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Cantoblanco, 28049 Madrid, Spain
2 Departamento de Genética, Facultad de Biología, Universidad Complutense de Madrid, 28040 Madrid, Spain

{ddagger} Author for correspondence (e-mail: julio.s.rufas{at}uam.es)

Accepted 21 March 2005

The relationship between meiotic recombination events and different patterns of pairing and synapsis has been analysed in prophase I spermatocytes of the grasshopper Stethophyma grossum, which exhibit very unusual meiotic characteristics, namely (1) the three shortest bivalents achieve full synapsis and do not show chiasma localisation; (2) the remaining eight bivalents show restricted synapsis and proximal chiasma localisation, and (3) the X chromosome remains unsynapsed. We have studied by means of immunofluorescence the localisation of the phosphorylated histone H2AX ({gamma}-H2AX), which marks the sites of double-strand breaks; the SMC3 cohesin subunit, which is thought to have a close relationship to the development of the axial element (a synaptonemal complex component); and the recombinase RAD51. We observed a marked nuclear polarization of both the maturation of SMC3 cohesin axis and the ulterior appearance of {gamma}-H2AX and RAD51 foci, these being exclusively restricted to those chromosomal regions that first form cohesin axis stretches. This polarised distribution of recombination events is maintained throughout prophase I over those autosomal regions that are undergoing, or about to undergo, synapsis. We propose that the restricted distribution of recombination events along the chromosomal axes in the spermatocytes is responsible for the incomplete presynaptic homologous alignment and, hence, for the partial synaptonemal complex formation displayed by most bivalents.

Key words: Double-strand breaks, Synapsis, Recombination, {gamma}-H2AX, Meiosis, RAD51




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