Abstract
Silene latifolia is a dioecious plant with heteromorphic XY sex chromosomes. Previous studies of sex chromosome–linked genes have suggested a gradual divergence between the X-linked and the Y-linked genes in proportion to the distance from the pseudoautosomal region. However, such a comparison has yet to be made for the noncoding regions. To better characterize the nonrecombining region of the X and Y chromosomes, we sequenced bacterial artificial chromosome clones containing the sex chromosome–linked paralogs SlAP3X and SlAP3Y, including 115 kb and 73 kb of sequences, respectively, flanking these genes. The synonymous nucleotide divergence between SlAP3X and SlAP3Y indicated that recombination stopped approximately 3.4 million years ago. Sequence homology analysis revealed the presence of six long terminal repeat retrotransposon-like elements. Using the nucleotide divergence calculated between left and right long terminal repeat sequences, insertion dates were estimated to be 0.083–1.6 million years ago, implying that all elements detected were inserted after recombination stopped. A reciprocal sequence homology search facilitated the identification of four homologous noncoding DNA regions between the X and Y chromosomes, spanning 6.7% and 10.6% of the X chromosome–derived and Y chromosome–derived sequences, respectively, investigated. Genomic Southern blotting and fluorescence in situ hybridization showed that the noncoding DNA flanking SlAP3X/Y has homology to many regions throughout the genome, regardless of whether they were homologous between the X and Y chromosomes. This finding suggests that most noncoding DNA regions rapidly lose their counterparts because of the introduction of transposable elements and indels (insertion–deletions) after recombination has stopped.
Highlights
Silene latifolia is a dioecious plant with heteromorphic XY sex chromosomes
Using several X-Y gene pairs, dates associated with recombination suppression have been estimated in species of mammals (Lahn and Page 1999), birds (Lawson-Handley et al 2004; Nam and Ellegren 2008), and plants [S. latifolia (Bergero et al 2007) and C. papaya (Wang et al 2012)], revealing differences in the estimated dates based on the chromosomal regions in which the pairs were located
By mapping eight X-linked genes, it has been reported that silent site divergence between X-Y gene pairs increased in proportion to the distance of the gene pair from the pseudoautosomal region (PAR), and it has been suggested that recombination between the X and Y chromosomes stopped in progressive steps that formed two evolutionary strata (Bergero et al 2007)
Summary
Previous studies of sex chromosome–linked genes have suggested a gradual divergence between the X-linked and the Y-linked genes in proportion to the distance from the pseudoautosomal region Such a comparison has yet to be made for the noncoding regions. SlAP3A was thought to be located on the autosome, because this gene was first detected by genomic PCR using SlAP3A-specific primers and flow-sorted X chromosomes and autosomes (Matsunaga et al 2003) It was later amplified by Cegan et al (2010) by using microdissected X chromosomes, but not microdissected autosomes; the gene has since been renamed SlAP3X. The divergence of noncoding regions is possibly a driving force behind the degeneration of X and Y chromosomes, resulting in differential expression of X-linked and Y-linked genes
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