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Disassembly of the synaptonemal complex in chicken oocytes analyzed by super-resolution microscopy

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Abstract

The synaptonemal complex is an evolutionarily conserved, supramolecular structure that holds the homologous chromosomes together during the pachytene stage of the first meiotic prophase. Among vertebrates, synaptonemal complex dynamics has been analyzed in mouse spermatocytes following the assembly of its components from leptotene to pachytene stages. With few exceptions, a detailed study of the disassembly of SCs and the behavior of SC components at recombination sites at the onset of diplotene has not been accomplished. Here, we describe for the first time the progressive disassembly of the SC in chicken oocytes during the initial steps of desynapsis using immunolocalization of specific SC proteins and super-resolution microscopy. We found that transverse filament protein SYCP1 and central element component SYCE3 remain associated with the lateral elements at the beginning of chromosomal axis separation. As the separation between lateral elements widens, these proteins eventually disappear, without any evidence of subsequent association. Our observations support the idea that post-translational modifications of the central region components have a role at the initial phases of the SC disassembly. At the crossover sites, signaled by persistent MLH1 foci, the central region proteins are no longer detected when the SYCP3-positive lateral elements are widely separated. These findings are indicative that SC disassembly follows a general pattern along the desynaptic bivalents. The present work shows that the use of avian oocytes at prophase I provides a valuable model to explore the time course and chromosomal localization of SC proteins and its relationship with local changes along meiotic bivalents.

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Acknowledgements

We would like to especially thank Prof. Dr. Alberto Solari for his continuous encouraging and helpful discussions, MSc. Mónica Rahn and MSSc C. Deparci for her helpful assistance, Dr. Teresa Klein for helpful counseling on SIM, and MSc. Irene da Cruz and Marcus Behringer for technical discussions on SIM techniques. We would also like to thank Prof. Dr. Manfred Alsheimer for the generous gift of SYCE3 antibody.

Funding

PIP1148CO from the National Council of Scientific and Technical Research (CONICET to R.B.S.-A.J.S.); Grant Be1168/8-1 from the German Science Foundation (to R.B.); BID-PICT 2016N° 2302 (ANPCyT to MIP); Research Stays for University Academics and Scientists (DAAD to RBS, 2017); International Scholarship for Young Researchers (CONICET to RBS, 2018).

Author information

Authors and Affiliations

  1. 2da. U.A. Biología Celular, Histología, Embriología y Genética, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina

    Roberta B. Sciurano

  2. Department of Cell and Developmental Biology, Biocenter, University of Würzburg, 97074, Würzburg, Germany

    Roberta B. Sciurano & Ricardo Benavente

  3. CONICET, Buenos Aires, Argentina

    Roberta B. Sciurano

  4. Instituto de Investigaciones Biomédicas, INBIOMED, CONICET-Universidad de Buenos Aires, Paraguay 2155, piso 10, C1121ABG, Buenos Aires, Argentina

    María Inés Pigozzi

Authors
  1. Roberta B. Sciurano
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  2. María Inés Pigozzi
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  3. Ricardo Benavente
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Contributions

RBS and MIP conceived the study; RBS, performed research; RBS, MIP, and RB analyzed the data and wrote the draft.

Corresponding authors

Correspondence to María Inés Pigozzi or Ricardo Benavente.

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The authors declare that they have no conflict of interest.

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This article is part of a Special Issue on “Recent advances in meiosis from DNA replication to chromosome segregation” edited by Valérie Borde and Francesca Cole, co-edited by Paula Cohen and Scott Keeney".

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Fig. S1

Measurements of the distance between axial elements in points I, II, III and IV of the macrochromosomes #3 and #8 at initial and advanced stages of chromosomes separation. Both macrochromosomes were straightened using the corresponding tool from the FIJI image software and four points (I, II, III and IV) were measured along the chromosomal axes. Those regions with twisted axes were discarded. Scale bars: 2 μm and 1 μm (insets) (PNG 1100 kb)

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Sciurano, R.B., Pigozzi, M.I. & Benavente, R. Disassembly of the synaptonemal complex in chicken oocytes analyzed by super-resolution microscopy. Chromosoma 128, 443–451 (2019). https://doi.org/10.1007/s00412-019-00693-w

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  • DOI: https://doi.org/10.1007/s00412-019-00693-w

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