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Protein markers of synaptic behavior and chromatin remodeling of the neo-XY body in phyllostomid bats

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Abstract

The XX/XY system is the rule among mammals. However, many exceptions from this general pattern have been discovered since the last decades. One of these non-conventional sex chromosome mechanisms is the multiple sex chromosome system, which is evolutionary fixed among many bat species of the family Phyllostomidae, and has arisen by a translocation between one original gonosome (X or Y chromosome), and an autosome, giving rise to a “neo-XY body.” The aim of this work is to study the synaptic behavior and the chromatin remodeling of multiple sex chromosomes in different species of phyllostomid bats using electron microscopy and molecular markers. Testicular tissues from adult males of the species Artibeus lituratus, Artibeus planirostris, Uroderma bilobatum, and Vampyrodes caraccioli from the eastern Amazonia were analyzed by optical/electron microscopy and immunofluorescence of meiotic proteins involved in synapsis (SYCP3 and SYCE3), sister-chromatid cohesion (SMC3), and chromatin silencing (BRCA1, γ-H2AX, and RNApol 2). The presence of asynaptic axes—labeled by BRCA1 and γ-H2AX—at meiotic prophase in testes that have a normal development of spermatogenesis, suggests that the basic mechanism that arrests spreading of transcriptional silencing (meiotic sex chromosome inactivation (MSCI)) to the autosomal segments may be per se the formation of a functional synaptonemal complex between homologous or non-homologous regions, and thus, this SC barrier might be probably related to the preservation of fertility in these systems.

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Acknowledgments

We specially thank MSSc. C. Deparci for her excellent assistance in EM techniques (UBA, Buenos Aires, Argentina), MSc. T.F.A. Ribas and Dr. A. J.B. Gomes (UFPA, Belem, Brazil) for capturing and handling animals, and Mg. Angie Barajas Ruiz (UBA, Buenos Aires, Argentina) for the technical assistance. We are also very grateful to Prof. M. Alsheimer (University of Würzburg, Germany) for the generous gift of SYCE3 antibody.

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Authors and Affiliations

  1. 2da. UA de Biología Celular, Histología, Embriología y Genética, Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155, Piso 10 (C1121ABG), Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina

    Mónica I. Rahn, Alberto J. Solari & Roberta B. Sciurano

  2. Laboratorio de Citogenética, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, PA, Brazil

    Renata C. Noronha, Cleusa Y. Nagamachi & Julio C. Pieczarka

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  1. Mónica I. Rahn
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  2. Renata C. Noronha
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  3. Cleusa Y. Nagamachi
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  4. Julio C. Pieczarka
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  5. Alberto J. Solari
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  6. Roberta B. Sciurano
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Correspondence to Roberta B. Sciurano.

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Funding

This study was funded by the Consejo Nacional de Investigaciones Científicas y Técnicas, CONICET (grant no. PIP11220120100683 to RBS and AJS), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação de Amparo à Pesquisa do Estado do Pará (FAPESPA) (Edital BIONORTE—grant no. Proc 552032/2010-7 to CYN and Edital Vale—grant no. Proc 2010/110447 to JCP).

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Fig. S1

The presence of multiple sex chromosomes in phyllostomid bats. a An electron micrograph of spermatocyte spread staining by phosphotungstic acid shows the presence of one recombination nodule (RN) in the long synaptonemal complex (SC) formed between the X and Y 2 chromosomes in Artibeus lituratus during pachytene stage (a RN in the shorter SC is not visible). k kinetochore. b–f The fluorescent immunolocalization of protein markers of synapsis and chromatin remodeling on pachytene spermatocyte spreads of the four analyzed species of phyllostomid bats reveal that (1) the cohesin SMC3 (b and d–f) and the SYCP3 protein of the lateral element of SC (c, red axes) are present on the single-chromosome axes in autosomes, as well as in multiple sex chromosomes; (2) the SYCE3 protein, a marker of the central element of SC, is located on synapsed regions (b, green axes); (3) the asynaptic axes of the sexual chromosomes are labeled by the DNA damage repair protein, BRCA1 (d, green axes), and the corresponding chromatin, by the phosphorylated variant histone, γ-H2AX (e, red area), indicating that these regions are transcriptionally silenced, as shown by the depletion of RNApol2 (f, asterisk). b–f Multiple sex chromosomes, white arrows; b CREST, kinetochores. Al, Artibeus lituratus; Ap, A. planirostris; Ub, Uroderma bilobatum; Vc, Vampyrodes caraccioli. Bars a 1 μm and b–f 3 μm. (GIF 192 kb)

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Rahn, M.I., Noronha, R.C., Nagamachi, C.Y. et al. Protein markers of synaptic behavior and chromatin remodeling of the neo-XY body in phyllostomid bats. Chromosoma 125, 701–708 (2016). https://doi.org/10.1007/s00412-015-0566-1

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