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Recombination changes at the boundaries of fully and partially sex-linked regions between closely related Silene species pairs.

ABSTRACT: The establishment of a region of suppressed recombination is a critical change during sex chromosome evolution, leading to such properties as Y (and W) chromosome genetic degeneration, accumulation of repetitive sequences and heteromorphism. Although chromosome inversions can cause large regions to have suppressed recombination, and inversions are sometimes involved in sex chromosome evolution, gradual expansion of the non-recombining region could potentially sometimes occur. We here test whether closer linkage has recently evolved between the sex-determining region and several genes that are partially sex-linked in Silene latifolia, using Silene dioica, a closely related dioecious plants whose XY sex chromosome system is inherited from a common ancestor. The S. latifolia pseudoautosomal region (PAR) includes several genes extremely closely linked to the fully Y-linked region. These genes were added to an ancestral PAR of the sex chromosome pair in two distinct events probably involving translocations of autosomal genome regions causing multiple genes to become partially sex-linked. Close linkage with the PAR boundary must have evolved since these additions, because some genes added in both events now show almost complete sex linkage in S. latifolia. We compared diversity patterns of five such S. latifolia PAR boundary genes with their orthologues in S. dioica, including all three regions of the PAR (one gene that was in the ancestral PAR and two from each of the added regions). The results suggest recent recombination suppression in S. latifolia, since its split from S. dioica.

SUBMITTER: Campos JL

PROVIDER: S-EPMC5345606 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Recombination changes at the boundaries of fully and partially sex-linked regions between closely related Silene species pairs.

Campos J L JL Qiu S S Guirao-Rico S S Bergero R R Charlesworth D D

Heredity 20161109 4

The establishment of a region of suppressed recombination is a critical change during sex chromosome evolution, leading to such properties as Y (and W) chromosome genetic degeneration, accumulation of repetitive sequences and heteromorphism. Although chromosome inversions can cause large regions to have suppressed recombination, and inversions are sometimes involved in sex chromosome evolution, gradual expansion of the non-recombining region could potentially sometimes occur. We here test whethe ...[more]

PMID: 27827389

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Project description:BackgroundThe evolution of sex chromosomes is often accompanied by gene or chromosome rearrangements. Recently, the gene AP3 was characterized in the dioecious plant species Silene latifolia. It was suggested that this gene had been transferred from an autosome to the Y chromosome.ResultsIn the present study we provide evidence for the existence of an X linked copy of the AP3 gene. We further show that the Y copy is probably located in a chromosomal region where recombination restriction occurred during the first steps of sex chromosome evolution. A comparison of X and Y copies did not reveal any clear signs of degenerative processes in exon regions. Instead, both X and Y copies show evidence for relaxed selection compared to the autosomal orthologues in S. vulgaris and S. conica. We further found that promoter sequences differ significantly. Comparison of the genic region of AP3 between the X and Y alleles and the corresponding autosomal copies in the gynodioecious species S. vulgaris revealed a massive accumulation of retrotransposons within one intron of the Y copy of AP3. Analysis of the genomic distribution of these repetitive elements does not indicate that these elements played an important role in the size increase characteristic of the Y chromosome. However, in silico expression analysis shows biased expression of individual domains of the identified retroelements in male plants.ConclusionsWe characterized the structure and evolution of AP3, a sex linked gene with copies on the X and Y chromosomes in the dioecious plant S. latifolia. These copies showed complementary expression patterns and relaxed evolution at protein level compared to autosomal orthologues, which suggests subfunctionalization. One intron of the Y-linked allele was invaded by retrotransposons that display sex-specific expression patterns that are similar to the expression pattern of the corresponding allele, which suggests that these transposable elements may have influenced evolution of expression patterns of the Y copy. These data could help researchers decipher the role of transposable elements in degenerative processes during sex chromosome evolution.

Project description:Silene latifolia represents one of the best-studied plant sex chromosome systems. A new approach using RNA-seq data has recently identified hundreds of new sex-linked genes in this species. However, this approach is expected to miss genes that are either not expressed or are expressed at low levels in the tissue(s) used for RNA-seq. Therefore other independent approaches are needed to discover such sex-linked genes.Here we used 10 well-characterized S. latifolia sex-linked genes and their homologs in Silene vulgaris, a species without sex chromosomes, to screen BAC libraries of both species. We isolated and sequenced 4 Mb of BAC clones of S. latifolia X and Y and S. vulgaris genomic regions, which yielded 59 new sex-linked genes (with S. vulgaris homologs for some of them). We assembled sequences that we believe represent the tip of the Xq arm. These sequences are clearly not pseudoautosomal, so we infer that the S. latifolia X has a single pseudoautosomal region (PAR) on the Xp arm. The estimated mean gene density in X BACs is 2.2 times lower than that in S. vulgaris BACs, agreeing with the genome size difference between these species. Gene density was estimated to be extremely low in the Y BAC clones. We compared our BAC-located genes with the sex-linked genes identified in previous RNA-seq studies, and found that about half of them (those with low expression in flower buds) were not identified as sex-linked in previous RNA-seq studies. We compiled a set of ~70 validated X/Y genes and X-hemizygous genes (without Y copies) from the literature, and used these genes to show that X-hemizygous genes have a higher probability of being undetected by the RNA-seq approach, compared with X/Y genes; we used this to estimate that about 30% of our BAC-located genes must be X-hemizygous. The estimate is similar when we use BAC-located genes that have S. vulgaris homologs, which excludes genes that were gained by the X chromosome.Our BAC sequencing identified 59 new sex-linked genes, and our analysis of these BAC-located genes, in combination with RNA-seq data suggests that gene losses from the S. latifolia Y chromosome could be as high as 30 %, higher than previous estimates of 10-20%.

Dataset Information

Recombination changes at the boundaries of fully and partially sex-linked regions between closely related Silene species pairs.

Publications

Recombination changes at the boundaries of fully and partially sex-linked regions between closely related Silene species pairs.

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