Strategies for meiotic sex chromosome dynamics and telomeric elongation in Marsupials.

Laia Marín-Gual,Paul D Waters,Gala Pujol,Jesús Page,Raúl Fernández-Donoso,Aurora Ruiz-Herrera,Soledad Berríos,Marta Martín-Ruiz,Covadonga Vara,Andrew Pask,Laura González-Rodelas,Marilyn B Renfree

doi:10.1371/journal.pgen.1010040

Abstract

During meiotic prophase I, homologous chromosomes pair, synapse and recombine in a tightly regulated process that ensures the generation of genetically variable haploid gametes. Although the mechanisms underlying meiotic cell division have been well studied in model species, our understanding of the dynamics of meiotic prophase I in non-traditional model mammals remains in its infancy. Here, we reveal key meiotic features in previously uncharacterised marsupial species (the tammar wallaby and the fat-tailed dunnart), plus the fat-tailed mouse opossum, with a focus on sex chromosome pairing strategies, recombination and meiotic telomere homeostasis. We uncovered differences between phylogroups with important functional and evolutionary implications. First, sex chromosomes, which lack a pseudo-autosomal region in marsupials, had species specific pairing and silencing strategies, with implications for sex chromosome evolution. Second, we detected two waves of γH2AX accumulation during prophase I. The first wave was accompanied by low γH2AX levels on autosomes, which correlated with the low recombination rates that distinguish marsupials from eutherian mammals. In the second wave, γH2AX was restricted to sex chromosomes in all three species, which correlated with transcription from the X in tammar wallaby. This suggests non-canonical functions of γH2AX on meiotic sex chromosomes. Finally, we uncover evidence for telomere elongation in primary spermatocytes of the fat-tailed dunnart, a unique strategy within mammals. Our results provide new insights into meiotic progression and telomere homeostasis in marsupials, highlighting the importance of capturing the diversity of meiotic strategies within mammals.

Highlights

A hallmark of sexual reproduction is the generation of haploid gametes with half the chromosome complement of progenitor cells by a complex, albeit tightly regulated, reductional cell division called meiosis
This is accomplished by a complex, albeit tightly regulated, reductional cell division called meiosis
Meiosis has been extensively studied in eutherian mammal model species, our understanding of the mechanisms regulating chromosome synapsis, recombination and segregation during meiosis progression is still incomplete especially in non-eutherian mammals

Summary

Introduction

A hallmark of sexual reproduction is the generation of haploid gametes with half the chromosome complement of progenitor cells by a complex, albeit tightly regulated, reductional cell division called meiosis. The mechanisms underlying meiotic progression have been extensively studied in model organisms, including yeast, fruit flies, nematodes, mice and, more recently, zebrafish [1,2] This has revealed canonical features that are conserved across large evolutionary time scales, including fundamental events such as the formation of double strand breaks (DSBs—essential for meiotic recombination), homologous chromosome pairing and synapsis, and the formation of the telomeric bouquet. Detailed immunofluorescence studies on chromosome pairing during prophase I in marsupials are scarce and restricted to a handful of American species [13,14] Due to their distant relationship with eutherian mammals, and that Australian and American species shared a common ancestor 80 Mya [15], marsupials offer a unique opportunity to explore previously uncharacterised meiotic features. This includes unique sex chromosome pairing strategies, recombination and meiotic telomeric homeostasis

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