Genomic identification and characterization of the pseudoautosomal region in highly differentiated avian sex chromosomes

Abstract

The molecular characteristics of the pseudoautosomal region (PAR) of sex chromosomes remain elusive. Despite significant genome-sequencing efforts, the PAR of highly differentiated avian sex chromosomes remains to be identified. Here we use linkage analysis together with whole-genome re-sequencing to uncover the 630-kb PAR of an ecological model species, the collared flycatcher. The PAR contains 22 protein-coding genes and is GC rich. The genetic length is 64 cM in female meiosis, consistent with an obligate crossing-over event. Recombination is concentrated to a hotspot region, with an extreme rate of >700 cM/Mb in a 67-kb segment. We find no signatures of sexual antagonism and propose that sexual antagonism may have limited influence on PAR sequences when sex chromosomes are nearly fully differentiated and when a recombination hotspot region is located close to the PAR boundary. Our results demonstrate that a very small PAR suffices to ensure homologous recombination and proper segregation of sex chromosomes during meiosis.

The Eutherian Pseudoautosomal Region

“…It is thought that the PAR exists because recombination is one of the essential mechanisms to ensure proper pairing and segregation of sex chromosomes during meiosis [Otto et al, 2011;Smeds et al, 2014]. This is consistent with studies in humans and mouse showing that the inhibition of recombination in the PAR is associated with an increased frequency of XY aneuploidy and male infertility [Kauppi et al, 2012;White et al, 2012].…”

“…Since then, molecular events such as inversions and transpositions have shaped the PAR by reducing XY homology, introducing new barriers to recombination, and moving the PAB [Iwase et al, 2003;Marais and Galtier, 2003;Park et al, 2005]. Overall, the PAR is a dynamic entity with a tendency to shrink as recombination suppression spreads Otto et al, 2011;Smeds et al, 2014]. Perhaps the only way to salvage this process is to have new autosomal additions to the sex chromosomes, as it has happened in collared lemmings, where a pair of autosomes has translocated to the X and Y creating a neo-XY sex chromosome system with a neo-PAR [Berend et al, 1997].…”

“…The key factor triggering this process has been gradually increased in mutation-led sequence differences that eventually hampered pairing and suppressed recombination around a sex-determining or sex-benefit locus, later spreading over other regions of the 2 chromosomes [Ohno, 1967;Charlesworth et al, 2005;Graves, 2006;Ming and Moore, 2007;Kaiser and Bachtrog, 2010;Ellegren, 2011;Otto et al, 2011;Smeds et al, 2014]. Suppressed recombination, in turn, led to genetic reduction and degeneration of the sex-specific chromosome, resulting in structurally and molecularly distinct sex chromosomes -the X and the Y in, for example, mammals, fruit flies and cucumbers, and the Z and the W in butterflies, lizards and birds [Jamilena et al, 2008;Kaiser and Bachtrog, 2010;Otto et al, 2011;Smeds et al, 2014].…”

Mammalian X homolog acts as sex chromosome in lacertid lizards

“…Table 1 Chromosomal position of the genes tested for differences in gene dose between sexes in the six-striped long-tailed lizard (Takydromus sexlineatus (TSE)), the green anole (Anolis carolinensis (ACA)), the chicken (Gallus gallus (GGA)) and human (Homo sapiens (HSA)) (Figure 1) of the identification of Z-or X-specific genes in organisms with degenerated unpaired sex chromosomes based on the combination of transcriptome analysis in a heterogametic individual and subsequent validation of candidates by qPCR technique proved to be reliable, relatively cheap and effective. However, we should keep in mind that it is not able to distinguish autosomal and pseudoautosomal regions (see, for example, Smeds et al, 2014;Zhang et al, 2015 for molecular approaches devoted to the analysis of gene content of pseudoautosomal regions). In addition, not all Z-or X-specific genes are lost from the degenerated W-and Y-specific region, respectively, and nonfunctional remnants of the ancestral genes (pseudogenes) may still persist in the degenerated part of the W or Y chromosomes (see Smeds et al, 2014).…”

“…However, we should keep in mind that it is not able to distinguish autosomal and pseudoautosomal regions (see, for example, Smeds et al, 2014;Zhang et al, 2015 for molecular approaches devoted to the analysis of gene content of pseudoautosomal regions). In addition, not all Z-or X-specific genes are lost from the degenerated W-and Y-specific region, respectively, and nonfunctional remnants of the ancestral genes (pseudogenes) may still persist in the degenerated part of the W or Y chromosomes (see Smeds et al, 2014). Such genes are likely to be heterozygous in transcriptome and thus filtered out in our analysis.…”