Relationship between sequence homology, genome architecture, and meiotic behavior of the sex chromosomes in North American Voles

Beth L. Dumont, Christina L. Williams, Bee Ling Ng, Valerie Horncastle, Carol L Chambers, Lisa A. McGraw, David Adams, Trudy F.C. Mackay, Matthew Breen

Research output: Contribution to journalArticle

Abstract

In most mammals, the X and Y chromosomes synapse and recombine along a conserved region of homology known as the pseudoautosomal region (PAR). These homology-driven interactions are required for meiotic progression and are essential for male fertility. Although the PAR fulfills key meiotic functions in most mammals, several exceptional species lack PAR-mediated sex chromosome associations at meiosis. Here, we leveraged the natural variation in meiotic sex chromosome programs present in North American voles (Microtus) to investigate the relationship between meiotic sex chromosome dynamics and X/Y sequence homology. To this end, we developed a novel, reference-blind computational method to analyze sparse sequencing data from flow-sorted X and Y chromosomes isolated from vole species with sex chromosomes that always (Microtus montanus), never (Microtus mogollonensis), and occasionally synapse (Microtus ochrogaster) at meiosis. Unexpectedly, we find more shared X/Y homology in the two vole species with no and sporadic X/Y synapsis compared to the species with obligate synapsis. Sex chromosome homology in the asynaptic and occasionally synaptic species is interspersed along chromosomes and largely restricted to low-complexity sequences, including a striking enrichment for the telomeric repeat sequence, TTAGGG. In contrast, homology is concentrated in high complexity, and presumably euchromatic, sequence on the X and Y chromosomes of the synaptic vole species, M. montanus. Taken together, our findings suggest key conditions required to sustain the standard program of X/Y synapsis at meiosis and reveal an intriguing connection between heterochromatic repeat architecture and noncanonical, asynaptic mechanisms of sex chromosome segregation in voles.

Original languageEnglish (US)
Pages (from-to)83-97
Number of pages15
JournalGenetics
Volume210
Issue number1
DOIs
StatePublished - Sep 1 2018

Fingerprint

Arvicolinae
Sex Chromosomes
Sequence Homology
Genome
Chromosome Pairing
Y Chromosome
Meiosis
X Chromosome
Synapses
Mammals
Chromosome Segregation
Fertility
Chromosomes

Keywords

  • Meiotic synapsis
  • Microtus heterochromatin
  • Pseudoautosomal region
  • Telomeric repeats

ASJC Scopus subject areas

  • Genetics

Cite this

Relationship between sequence homology, genome architecture, and meiotic behavior of the sex chromosomes in North American Voles. / Dumont, Beth L.; Williams, Christina L.; Ng, Bee Ling; Horncastle, Valerie; Chambers, Carol L; McGraw, Lisa A.; Adams, David; Mackay, Trudy F.C.; Breen, Matthew.

In: Genetics, Vol. 210, No. 1, 01.09.2018, p. 83-97.

Research output: Contribution to journalArticle

Dumont, BL, Williams, CL, Ng, BL, Horncastle, V, Chambers, CL, McGraw, LA, Adams, D, Mackay, TFC & Breen, M 2018, 'Relationship between sequence homology, genome architecture, and meiotic behavior of the sex chromosomes in North American Voles', Genetics, vol. 210, no. 1, pp. 83-97. https://doi.org/10.1534/genetics.118.301182
Dumont, Beth L. ; Williams, Christina L. ; Ng, Bee Ling ; Horncastle, Valerie ; Chambers, Carol L ; McGraw, Lisa A. ; Adams, David ; Mackay, Trudy F.C. ; Breen, Matthew. / Relationship between sequence homology, genome architecture, and meiotic behavior of the sex chromosomes in North American Voles. In: Genetics. 2018 ; Vol. 210, No. 1. pp. 83-97.
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