TY - JOUR
T1 - Relationship between sequence homology, genome architecture, and meiotic behavior of the sex chromosomes in North American Voles
AU - Dumont, Beth L.
AU - Williams, Christina L.
AU - Ng, Bee Ling
AU - Horncastle, Valerie
AU - Chambers, Carol L.
AU - McGraw, Lisa A.
AU - Adams, David
AU - Mackay, Trudy F.C.
AU - Breen, Matthew
N1 - Funding Information:
We thank Mary Ann Handel, Laura Reinholdt, Tanmoy Bhattacharyya, and Ewelina Bolcun-Filas for constructive feedback on analyses. This work was supported by a K99/ R00 Pathway to Independence Award from the National Institute of General Medical Sciences (GM110332 to B.L.D.).
Publisher Copyright:
© 2018 by the Genetics Society of America.
PY - 2018/9
Y1 - 2018/9
N2 - 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.
AB - 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.
KW - Meiotic synapsis
KW - Microtus heterochromatin
KW - Pseudoautosomal region
KW - Telomeric repeats
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U2 - 10.1534/genetics.118.301182
DO - 10.1534/genetics.118.301182
M3 - Article
C2 - 30002081
AN - SCOPUS:85052645535
VL - 210
SP - 83
EP - 97
JO - Genetics
JF - Genetics
SN - 0016-6731
IS - 1
ER -