Early Events in the Evolution of the <i>Silene latifolia</i> Y Chromosome: Male Specialization and Recombination Arrest

Žlůvová, Jitka; Georgiev, S.; Janoušek, Bohuslav; Charlesworth, Deborah; Vyskot, Boris; Negrutiu, Ioan

doi:10.1534/genetics.107.071175

Cited by 39 publications

(44 citation statements)

References 70 publications

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“…latifolia PAR: Unlike the previously published map, which used dominant AFLP markers and inferred two PARs (Scotti and Delph 2006;Delph et al 2010), our map, with a new set of mostly codominant markers, finds only a single PAR. This suggests that more study is needed before the existence of a second PAR is accepted, particularly as cytological studies consistently report terminal pairing of the X and Y chromosomes (e.g., Zluvova et al 2007;Filatov et al 2008), except in chromosome mutants (e.g., Westergaard 1946Westergaard , 1948aZluvova et al 2007). Both the previous mapping and ours, including families other than the mapping family, find a PAR of 25-30 cM (Figure 2, Table 3).…”

Section: Genetic Map Of S Latifoliamentioning

confidence: 62%

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Bergero

Qiu

Forrest³

et al. 2013

Genetics

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There are two very interesting aspects to the evolution of sex chromosomes: what happens after recombination between these chromosome pairs stops and why suppressed recombination evolves. The former question has been intensively studied in a diversity of organisms, but the latter has been studied largely theoretically. To obtain empirical data, we used codominant genic markers in genetic mapping of the dioecious plant Silene latifolia, together with comparative mapping of S. latifolia sex-linked genes in S. vulgaris (a related hermaphrodite species without sex chromosomes). We mapped 29 S. latifolia fully sex-linked genes (including 21 newly discovered from transcriptome sequencing), plus 6 genes in a recombining pseudo-autosomal region (PAR) whose genetic map length is 25 cM in both male and female meiosis, suggesting that the PAR may contain many genes. Our comparative mapping shows that most fully sex-linked genes in S. latifolia are located on a single S. vulgaris linkage group and were probably inherited from a single autosome of an ancestor. However, unexpectedly, our maps suggest that the S. latifolia PAR region expanded through translocation events. Some genes in these regions still recombine in S. latifolia, but some genes from both addition events are now fully sex-linked. Recombination suppression is therefore still ongoing in S. latifolia, and multiple recombination suppression events have occurred in a timescale of few million years, much shorter than the timescale of formation of the most recent evolutionary strata of mammal and bird sex chromosomes. It is now understood that the large nonrecombining regions of sex chromosomes in mammals have expanded over evolutionary time, forming "evolutionary strata" with differing levels of sequence divergence between X-and Y-gene pairs, from ancient highly diverged regions, to regions in which the genes started diverging much more recently, which are located closest to the pseudo-autosomal region (PAR) on the X chromosome genetic and physical maps (Lahn and Page 1999;Skaletsky et al. 2003;Marais et al. 2008). The more recent evolutionary strata were formed by recombination suppression in regions formed by an addition of autosomal genetic material to the sex chromosomes (Waters et al. 2001), demonstrating that suppressed recombination spread from the ancestral sex chromosomal region into initially recombining regions. The PAR is shared across Eutherian mammals (despite differences in its boundary and the recent addition of a second PAR, PAR2, in humans), which is a physically small remnant of the added region, which is still autosomal in marsupials (Waters et al. 2001).The major current explanation for the evolution of expanded nonrecombining regions of sex chromosomes is

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Section: Genetic Map Of S Latifoliamentioning

confidence: 62%

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Bergero

Qiu

Forrest³

et al. 2013

Genetics

Self Cite

122

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“…Expression studies may also help to identify sex-determining genes in S. latifolia, about which we still know very little, despite having some knowledge of the pathways involved in the floral developmental programs in Silene (Zluvova et al, 2007) and the Y chromosomal regions involved in maledetermination (Lardon et al, 1999;Lebel-Hardenack et al, 2002;Bergero et al, 2008).…”

Section: Sex Chromosome Evolutionmentioning

confidence: 99%

Silene as a model system in ecology and evolution

et al. 2009

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The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data. The model role of a non-model organismThe genus Silene (Caryophyllaceae), with a tradition of genetical and ecological studies dating back to Mendel and Darwin, has remarkably many interesting features. First, the species in the genus vary widely in their breeding systems and ecology. Second, several members of this mainly holarctic genus can be easily bred, and have short life cycles, and are thus convenient for experimental and field studies. Genomic resources are now becoming increasingly available in Silene, making genetic, quantitative genetic and molecular studies possible. A strength of Silene as a model system, compared with many classical model organisms, is that researchers can rely on a large number of ecological studies encompassing biotic interactions with sexually transmitted fungi, pollinators and herbivores. It is the wealth of ecological and other earlier knowledge that makes the genus Silene important for studying many biological questions, including the suppression of recombination during sex chromosome evolution, sexually antagonistic selection in an organism that is not an animal, epigenetic processes in flower development, speciation and reproductive isolation, multi-trophic interactions, disease ecology and biological invasions.Thanks to the classical genetic and ecological work on Silene, new progress can now be made in studying some of these important unresolved questions in biology with the aid of modern molecular tools. That new model systems with accessible and well-studied ecology open fruitful avenues for investigation is illustrated also by Mimulus (Wu et al., 2008) and the ongoing efforts to develop genomic resources in an increasing number of different systems. In the following, we outline the unique features of the Silene system, and describe active research areas and future directions, highlighting new advances and work in progress. Evolution of sexual systemsPlants show remarkable diversity in their sexual and mating systems, ranging from hermaphroditism to dioecy, from self-incompatible hermaphroditism to hermaphroditism in which individuals possess a capacity to self-fertilize, but which often show complex mechanisms to promote outcrossing (Darwin, 18...

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“…Other deletions cause male sterility, and cytogenetic studies show that these can involve either arm of the Y (Westergaard 1958;Farbos et al 1999;Lardon et al 1999), suggesting at least one locus on each arm (Zluvova et al 2007); defects in the latest stages of anther development clearly involve Yq arm deletions (see below for more details). However, there are some inconsistencies.…”

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confidence: 99%

“…The explanation for this, and other inconsistencies in the map, has so far been that these strains have undergone two deletions or, for many deletion strains, even more than two, but there is no independent evidence for this from the cytology. Since deletions are expected to be rare events and are indeed found only rarely among the S. latifolia progeny plants derived from pollinations using irradiated pollen (Zluvova et al 2007), it is expected that most strains should have single deletions, so that multiple deletions seem unlikely. Data on the distribution of numbers of deletions are scarce, and different plants might differ in this respect, but a study of deletions in a set of 55 chromosomes in girradiated maize (a plant whose genome size is very similar to that of S. latifolia), in which the frequency of deletions was very high (29 had one or more deletions), found 18 with single deletions and 11 with more than one [the maximum numbers were high, with one strain having five deletions, and one six (Riera-Lizarazu et al 2000)].…”

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confidence: 99%

Defining Regions and Rearrangements of the Silene latifolia Y Chromosome

et al. 2008

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We combine data from published marker genotyping of three sets of S. latifolia Y chromosome deletion mutants with changed sex phenotypes and add genotypes for several new genic markers to refine the deletion map of the Y chromosome and compare it with the X chromosome genetic map. We conclude that the Y chromosome of this species has been derived through multiple rearrangements of the ancestral gene arrangement and that none of the rearrangements so far detected was involved in stopping X-Y recombination. Different Y genotypes may also differ in their gene content and possibly arrangements, suggesting that mapping the Y-linked sex-determining genes will be difficult, even if many further genic markers are obtained. Even in determining the map of Y chromosome markers to discover all the rearrangements, physical mapping by FISH or other experiments will be essential. Future deletion mapping work should ensure that markers are studied in the parents of deletion mutants and should probably include additional deletions that were not ascertained by causing mutant sex phenotypes.

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Early Events in the Evolution of the Silene latifolia Y Chromosome: Male Specialization and Recombination Arrest

Cited by 39 publications

References 70 publications

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Expansion of the Pseudo-autosomal Region and Ongoing Recombination Suppression in the Silene latifolia Sex Chromosomes

Silene as a model system in ecology and evolution

Defining Regions and Rearrangements of the Silene latifolia Y Chromosome

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