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Disentangling the effects of mating systems and mutation rates on cytoplasmic [correction of cytoplamic] diversity in gynodioecious Silene nutans and dioecious Silene otites.

ABSTRACT: Many flowering plant species exhibit a variety of distinct sexual morphs, the two most common cases being the co-occurrence of females and males (dioecy) or the co-occurrence of hermaphrodites and females (gynodioecy). In this study, we compared DNA sequence variability of the three genomes (nuclear, mitochondrial and chloroplastic) of a gynodioecious species, Silene nutans, with that of a closely related dioecious species, Silene otites. In the light of theoretical models, we expect cytoplasmic diversity to differ between the two species due to the selective dynamics that acts on cytoplasmic genomes in gynodioecious species: under an epidemic scenario, the gynodioecious species is expected to exhibit lower cytoplasmic diversity than the dioecious species, while the opposite is expected in the case of balancing selection maintaining sterility cytoplasms in the gynodioecious species. We found no difference between the species for nuclear gene diversity, but, for the cytoplasmic loci, the gynodioecious S. nutans had more haplotypes, and higher nucleotide diversity, than the dioecious relative, S. otites, even though the latter has a relatively high rate of mitochondrial synonymous substitutions, and therefore presumably a higher mutation rate. Therefore, as the mitochondrial mutation rate cannot account for the higher cytoplasmic diversity found in S. nutans, our findings support the hypothesis that gynodioecy in S. nutans has been maintained by balancing selection rather than by epidemic-like dynamics.

SUBMITTER: Lahiani E

PROVIDER: S-EPMC3716271 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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Disentangling the effects of mating systems and mutation rates on cytoplasmic [correction of cytoplamic] diversity in gynodioecious Silene nutans and dioecious Silene otites.

Lahiani E E Dufaÿ M M Castric V V Le Cadre S S Charlesworth D D Van Rossum F F Touzet P P

Heredity 20130417 2

Many flowering plant species exhibit a variety of distinct sexual morphs, the two most common cases being the co-occurrence of females and males (dioecy) or the co-occurrence of hermaphrodites and females (gynodioecy). In this study, we compared DNA sequence variability of the three genomes (nuclear, mitochondrial and chloroplastic) of a gynodioecious species, Silene nutans, with that of a closely related dioecious species, Silene otites. In the light of theoretical models, we expect cytoplasmic ...[more]

PMID: 23591518

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Project description:BACKGROUND:Gynodioecious species exist in two sexes - male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about sex-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes. RESULTS:We generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two sexes. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study. CONCLUSIONS:We revealed no significant differences between the sexes in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both sexes may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

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

Disentangling the effects of mating systems and mutation rates on cytoplasmic [correction of cytoplamic] diversity in gynodioecious Silene nutans and dioecious Silene otites.

Publications

Disentangling the effects of mating systems and mutation rates on cytoplasmic [correction of cytoplamic] diversity in gynodioecious Silene nutans and dioecious Silene otites.

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