Abstract Background




Дата канвертавання26.04.2016
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Abstract

Background:

Silene latifolia has become a model for the study of plant sex chromosome evolution. This species has a sex chromosome system similar to mammals, with females being homogametic (XX) and males heterogametic (XY). While mammalian sex chromosomes present an evolutionary old system with sex chromosomes that emerged 150 million years ago (mya), the S. latifolia sex chromosomes emerged about 10 mya. Silene vulgaris is a closely related species of S. latifolia that lacks sex chromosomes. Comparisons between these plant species allow investigating early steps of the evolution of X and Y chromosomes in plants. We present in this study, an analysis of homologous BAC sequences identified on the S. latifolia X and Y chromosomes and the corresponding S. vulgaris autosomes, and we report the location of several newly identified sex-linked genes.

Results:

We identified 24 BAC clones containing known sex-linked genes and discovered 17 new sex-linked genes and 51 S. vulgaris autosomal genes that are potentially S. latifolia sex-linked gene homologs. In addition, we localized 59 recently discovered sex-linked genes and estimated positions of 31 others. Moreover, we found 18 new gene triplets (S. latifolia X, Y and S. vulgaris autosomal homologs). Structural analysis revealed small-scale collinearity conserved between genes close to S. latifolia SlX6a, a gene located in the oldest evolutionary stratum. BAC sequence assembly allowed to physically map genes for which only genetic maps were so far available and allowed us to identified the subtelomeric region of the S. latifolia X chromosome q-arm.



Conclusions:

The present study demonstrates the strength of combining BAC library analyses and next generation sequencing in a comparative approach. The notable absence of detectable pseudogenes on the Y chromosome and the homogeneous distribution of genes with reduced expression of the Y-linked allele along the X chromosome suggest that gene loss on the Y chromosome is rare and that inactivation of Y-linked gene copies is random in Silene latifolia.


Keywords: BAC library, next generation sequencing, sex chromosomes, Silene

Introduction

Silene latifolia sex chromosomes have emerged about 10 million years ago . While S. latifolia sex chromosomes are about fifteen times younger than mammalian sex chromosomes , several similarities have been found between both systems. First, Silene latifolia has heteromorphic sex chromosomes with females being the homogametic sex (XX) and males the heterogametic sex (XY). Degeneration of the S. latifolia Y chromosome is evidenced by the lethality of YY and Y0 mutants , reduced expression of Y alleles , accumulation of transposable elements (TE) and insertion of chloroplastic DNA . As previously found in human sex chromosomes , the suppression of recombination between S. latifolia X and Y chromosomes is a gradual process led by chromosomal rearrangements such as inversions, which resulted in formation of evolutionary strata . Recently, dosage compensation has been detected in S. latifolia showing an equal dosage of X transcripts for some genes in both males and females, similar to the situation in mammals .

The major limitation for the analysis of the sex chromosomes in Silene was until recently the availability of sex-linked genes. During the last decade, only about ten genes were identified on S. latifolia sex chromosomes . However, with the expansion of next generation sequencing technologies, new sex-linked genes were recently identified. Indeed, next-generation sequencing methods based on cDNA sequencing facilitated the collection and analysis of large numbers of Silene gene sequences and identification of novel putatively sex-linked genes . A major limitation of these approaches for the study of sex chromosome evolution is that the identification of sex-linked genes depends on the presence of male-specific polymorphisms. So the sex linked genes with well-preserved Y allele would not be detected. Similarly these approaches can identify hemizygous X-linked genes, but they cannot inform us whether the Y allele have been lost or silenced.

We therefore used a different approach based on sequencing selected bacterial artificial chromosome (BAC) clones. This method is highly demanding in terms of time and resources needed to develop and screen BAC libraries, compared to cDNA sequencing for example with the mRNA-seq approach. However, our approach possesses several advantages: It allows detecting weakly expressed genes and pseudogenes. It enables to identify the exon/intron structure, the linear arrangement of genes and also to analyze the intergenic regions. A combination of both cDNA library and BAC sequencing can further confirm sex-linkage of some of the newly obtained genes. Moreover, BAC analysis allows inferring the genes position regarding to the strata. So with the expression data provided by the cDNA libraries, we can test whether genes with reduced expression of the Y-allele and dosage compensated genes occur preferentially in the oldest strata that contain the most differentiated genes .

Here we report the results of a genomic comparison between sequences of 24 BAC clones coming from S. latifolia X and Y chromosomes and S. vulgaris homologous autosomes.



Material and Methods

BAC preparation

BACs were prepared following the methods described by Blavet et al. (in review) and Čegan et al. (2010) . The genes used to screen the BAC library are listed on Table 1.



Table 1: Sex-linked genes used to screen the BAC library.

Gene name

Information

References

SlX1

WD repeat protein




SlXDD44

Oligomycin sensitivity-conferring protein




Slss

Spermidine synthase




SlX3

Putative calcium dependent protein kinase




SlX4

Fructose-2,6-biphosphatase




SlX6a

Unknown protein




SlX6b

Unknown protein




SlX7

Unknown protein




SlXCyp

Peptidyl-prolyl cis-trans isomerase



In order to analyze selected regions along the S. latifolia sex chromosomes and the corresponding regions on the S. vulgaris autosomes, we first screened a BAC library of S. latifolia with different genes that were previously found to be located on the X chromosome (see Table 1) and have successfully been used for linkage mapping of the S. latifolia sex chromosomes . BAC sequencing was performed by 454 pyrosequencing (Roche). From these sequences we identified new genes and used them to screen a S. vulgaris BAC library for homologous clones. The Silene latifolia BAC library was screened again with new genes to detect their Y copies. All BAC sequences were assembled into contigs using GS De Novo Assembler (Roche).



Sequencing, assemblies and annotations

All 454 sequences were de novo assembled using Roche GS De Novo Assembler with 98% minimum overlap identity and 60 bp as minimum overlap length. We set the expected depth parameter with reference to the estimated size of the BAC (determined by pulse field gel electrophoresis (PFGE)) and the number of reads sequenced.

The contigs were annotated by similarity using BLAST with UniProtKB (Swiss-Prot + TrEMBL, 13 July 2010), the Arabidopsis thaliana proteome (TAIR10_20100802), S. latifolia cDNA contigs and transposable elements (TAIR9_TE) [www.arabidopsis.org] with an E-value cut-off of 1E-4. We also used a Silene repeated element database to detect Silene-specific repeats and transposable elements. Transposable element annotations were then completed using annotated S. latifolia repeats . After BLAST identification of Illumina contigs built by Muyle et al. (2012) , we used gene expression data to test whether gene expression patterns differ among the evolutionary strata. Statistical analyses were performed with R . Moreover we used both BAC and Illumina sequence read alignments to estimate numbers of both non-synonymous and synonymous substitutions for all genes.

Results

BAC sequencing, assembly and annotations

The 454 sequence reads of S. latifolia and S. vulgaris BAC clones were assembled in contigs and a total of 158 genes were identified through BLAST searches. Among the identified genes, we detected 90 genes that were recently identified as sex-linked genes by cDNA sequencing , with 59 and 31 of these being localized on S. latifolia and S. vulgaris BACs, respectively. In addition we found 17 new sex-linked genes and 51 S. vulgaris genes that potentially possess sex-linked homologs in S. latifolia. Among the identified genes, 18 triplets (homologous gene copies from S. latifolia X and Y chromosomes, and S. vulgaris autosome) were found. A total of 362 transposable or repeated elements were identified, as indicated by their annotations with Uniprot (www.uniprot.org) and repeat coverage. The repeat coverage is based on BLAST hits to a Silene repeated elements library .



Sex chromosome structure and comparison

Large-scale collinearity between the S. latifolia X chromosome and S. vulgaris autosome has repeatedly been reported in studies of S. latifolia sex chromosome evolution . This collinearity was evidenced by genetic mapping. With the development of genomic resources, small-scale collinearity can be analyzed at much higher resolution. In the present study we report the assembly of the BACs containing the genes SlX6a, SlX7 and SlX4 located on the X chromosome. We physically linked these genes that were expected to be close to each other based on earlier genetic mapping results . Then we evidenced collinearity of these genes with copies on the S. latifolia Y chromosome and S. vulgaris autosomes (Figure 1). Presence of X-43.1. tandem repeat close to the SlX4 gene suppose the proximity of telomeric region (Figure 1). Y copies of Sl4 and Sl7 genes are localized in large regions (150 kb and 205 kb) missing any other genes, instead several transposable elements are present along the sequences (Supplementary Figure 1).



Figure 1: Schematic representation of sex-linked gene arrangement. Gray rectangles indicate known sex-linked genes: 7 = SlX7, 6a = SlX6a and 4 = SlX4. White rectangles indicate newly discovered sex-linked genes. The rectangle with diagonal lines indicates X43.1. tandem repeat that is typical for S. latifolia telomeres.


Pseudogene investigation

The identified X-linked genes were used to search for pseudogenes on the Y chromosome derived BAC clones. For several genes in close proximity to genes SlX4, SlX6a and SlX7 on X-derived BAC clones, we have not detected any Y copies on BAC clones containing the genes SlY4 and SlY7. We used protein sequences determined from available cDNA reads and open reading frame (ORF) predictions from prot4EST for each X-linked gene in order to detect partial Y-linked copies, but none were identified.



Table 2: Sex-biased gene expression. Gene expression and dosage compensation are inferred from the results of Muyle et al. (2012) .

Stratum

Number of analyzed genes

Genes with reduced Y expression

Dosage compensated genes

1

7

5

0

2

20

13

3

3

11

7

4


Gene expression and dosage compensation

With the recent results on dosage compensation in S. latifolia evidenced by Muyle et al. (2012) , we assessed both the distribution of expression patterns and dosage compensated expression of the newly identified sex-linked genes with respect to their location in different evolutionary strata along the X chromosome. Table 2 presents the results of the expression analyses for genes located on the investigated BAC clones and indicates qualitatively the evidence for dosage compensation. We found that the distribution among evolutionary strata along the X chromosome is random for sex-linked genes that have a reduced expression of their Y allele (χ2 = 0.255, df = 2, p-value = 0.8803) and that are dosage compensated (χ2 = 4.0929, df = 2, p-value = 0.1292). Moreover, no significant difference exists in the average level of Y allele expression reduction among the genes from the different strata (anova: p-value = 0.8005).



Non-synonymous and synonymous substitutions

Using RNA-seq reads from Muyle and coworkers in combination with our BAC sequences, we analyzed substitution patterns of the genes for which we have copies from the S. latifolia X and Y chromosomes and the S. vulgaris autosomes. For the 18 gene triplets identified, we counted non-synonymous and synonymous substitutions occurring in both the X and Y alleles using S. vulgaris as outgroup (Table 3). Most non-synonymous mutations occurred in the alleles located on the Y chromosomes (2.3 and 2.6 times more on average than on the X for non-synonymous and synonymous mutations respectively) and are most common in genes in stratum 1, significantly for synonymous mutations (χ2 = 7.2275, df = 2, p-value = 0.02695) but not significantly for non-synonymous mutations (χ2 = 3.98, df = 2, p-value = 0.1367).



Table 3: Non-synonymous and synonymous substitutions in the different gene triplets. The genes are sorted according to their positions along the X chromosome. Strata are separated by dashed lines. NS = non-synonymous substitutions; SS = synonymous substitutions.

Name

BAC

Length

NS

SS

X

Y

X

Y

X

Y

Contig_29617

4

253

253

0

1

0

1

XY4 (Contig_29527)

4

370

360

8

15

15

28

gene_50 (Contig_1767)

6

464

234

1

14

3

56

gene_79 (Contig_62587)

7

784

451

9

50

25

119

XY7 (Contig_1849)

7

363

361

8

11

16

31

XY3 (Contig_49583)

3

158

253

11

6

28

14

Total stratum 1










37

97

87

249

Contig_61876-64482

dd44

354

354

1

0

2

1

XYDD44 (Contig_60039)

dd44

108

107

1

2

1

1

Xyss (Contig_8045)

ss

347

342

2

11

4

8

Contig_3463

cyp

1028

1028

2

5

8

8

Contig_53812

cyp

222

222

0

3

0

0

Contig_53821

cyp

106

106

0

1

0

0

Contig_58571

cyp

450

450

2

4

1

4

Contig_59644

cyp

148

148

0

0

4

6

Contig_63486

cyp

367

367

1

2

0

1

XYCyp (Contig_53905)

cyp

639

639

6

11

10

18

Total stratum 2










15

39

30

47

Contig_22623

1

86

86

0

0

0

0

Contig_44823

1

543

543

0

2

0

2

Contig_48921

1

165

165

0

0

0

2

Contig_53010

1

680

680

1

1

0

2

Contig_53773

1

129

129

0

0

0

1

Contig_59073

1

835

833

2

5

4

18

Contig_6732

1

820

729

3

4

3

7

XY1 (Contig_55531)

1

133

317

5

0

1

3

Total stratum 3










11

12

8

35

Total










63

148

125

331


Discussion

Y chromosome enlargement and weak gene loss

The comparison between the different BAC sequences revealed new evidence for small-scale gene collinearity and enlargement of the Y chromosome by insertion of transposable elements and showed that gene loss on the Y chromosome is reduced in comparison to much older sex chromosomes such as those of humans . We found that both genes, SlY4 and SlY7, are isolated, without any other gene located in close proximity, on their respective BACs (which are more than 150 kb in size), whereas other genes were localized in close proximity to the X copies of these genes (about 2 kb and 1 kb for the closest gene to SlX4 and SlX7, respectively). Moreover, no pseudogenes, resulting from the degeneration of the neighboring X-copy genes, has been detected on the Y chromosome which may indicate that S. latifolia Y-linked gene loss is very weak, as suggested from recent RNA-seq analysis . Both results imply that massive insertion of transposable elements in the intergenic regions between Y-linked gene copies contributed to the growth of the Y chromosome and separated neighboring genes (see Additional Figure 1). This scenario is supported by our finding of numerous transposable elements on Y-derived BACs. The insertion of transposable elements is known to be one of the main causes of sex chromosome degeneration and enlargement . S. latifolia Y chromosome is about 7.5 times larger than the S. vulgaris autosome . Here we described intergenic regions that have been enlarged more than 70 times. Compared to the moderate enlargement discovered in the pseudoautosomal region of the sex chromosome , the present result suggest that some regions of the S. latifolia Y chromosome have been differentially invaded by transposable elements and that TE invasion is strongest in that part of the chromosome where recombination stopped first during the evolution of the sex chromosomes.



Inactivation of Y-linked alleles

While evolutionary strata can readily be identified based on synonymous site divergence between X and Y-linked gene copies and are commonly found in many sex chromosome systems, patterns of X/Y allele expression divergence are less clear. A recent study in S. latifolia revealed that most of the Y-linked gene copies remain active, nevertheless, the expression level is about 87% compared to the X alleles . However, the physical localization of the studied genes is unknown. Using expression data of the genes located on our BACs in the different strata, we could test the hypothesis that reduced expression of Y-linked alleles is strongest in the oldest stratum. Contrary to expectations, our results suggest that genes of the Y chromosome are randomly inactivated. Thus, our results for the evolutionary young S. latifolia Y chromosome resemble those obtained for the Drosophila miranda neo-Y chromosome, for which a random model of gene inactivation was inferred .

Three models have been proposed for the inactivation of Y-linked allele expression: first, the direct model, in which genes that are nonfunctional on the Y (due to frameshift mutations) are targeted for inactivation ; second, the random model, in which genes are inactivated randomly with respect to their functionality on the Y, independent of frameshift mutations or transposable element insertions ; and third, the large-scale inactivation model, according to which large genomic regions are silenced simultaneously . For S. latifolia, we can exclude the direct model, because sequence divergence is most pronounced in the oldest stratum and inactivation would be preferentially found there. In addition, dosage compensation would be expected to occur on this stratum. Secondly, the large-scale inactivation model does not seem to explain the patterns of expression we observed. If S. latifolia Y chromosome evolution would follow this model, we should see inactivation, and then dosage compensation happening on neighboring genes, which is not the case. Finally, our results that show no preferential localization of genes with reduced Y expression suggest that the Y chromosome is more probable to follow a random inactivation process such as Drosophila miranda one .

Mutation rate and relaxed purifying selection

Our analysis of the distribution of non-synonymous and synonymous substitution provides new evidence for degeneration of Y chromosome-linked genes. Previous comparison of dN/dS ratios (nonsynonymous/synonymous substitution rates) between both X and Y alleles of S. latifolia sex-linked genes evidenced degeneration of the Y copies and revealed that these genes are evolving under purifying selection . While the analysis conducted by Marais and coworkers was limited to seven well characterized genes , the recent study conducted by Chibalina and Filatov was based on about 400 sex-linked genes characterized by RNA-seq, but for which location is still unknown . Our results enlarge the set of sex-linked genes with known locations in the different strata. We found an accumulation of both non-synonymous and synonymous substitutions in Y-linked alleles, preferentially in stratum one. Such pattern could result from a higher mutation rate on the Y chromosome . Purifying selection should eliminate deleterious non-synonymous substitutions. However, we observed that Y-linked genes accumulate more non-synonymous substitution compared to the X-linked copies, what could support the hypothesis that relaxed purifying selection occurs on the Y chromosome . This trend is most pronounced in the oldest stratum one.



Conclusions

In this study we present the analysis of several BAC sequences from S. latifolia X and Y chromosomes and S. vulgaris autosome. Each of the three evolutionary strata identified on S. latifolia sex chromosomes are represented in the BAC sequences. The analysis of the BAC sequences revealed the location of 76 sex-linked genes and showed a new case of collinearity between the different chromosomes of both Silene species, as well as a new example of massive transposable element insertion occurring on the Y chromosome. Y-linked genes with a reduced expression are randomly distributed in the different strata, what suggests an accidental inactivation of the Y-linked genes. Absence of pseudogenes may indicate a weak process of gene loss on the S. latifolia Y chromosome. Further the analysis of substitutions confirms both a higher mutation rate on the Y chromosome and the hypothesis of a relaxed purifying selection on S. latifolia Y chromosome. More important effect was revealed on the most diverged stratum one.



Acknowledgements

We thank L. Poveda, M. Kuenzli and W. Qi from the Functional Genomic Center Zurich (FGCZ) for assistance relating to 454 sequencing, T. Torossi, C. Michel and the ETH Zürich Genetic Diversity Center (GDC) for technical support, and S. Zoller for bioinformatics support. We further acknowledge support by J. Macas and E. Kejnovský who provided sequences of repeated elements and J. Bartoš who participated in BAC library analysis. This study was supported by an ETH Zurich grant (TH-07 06-3) to AW, by Czech Science Foundation grants (522/09/0083) to RH and Centre of the Region Haná for Biotechnological and Agricultural Research grant (ED0007/01/01) to RH.



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