Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Qiu, Suo; Bergero, Roberta; Charlesworth, Deborah

doi:10.1534/genetics.113.152397

Cited by 55 publications

(76 citation statements)

References 77 publications

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“…The accompanying article in this issue, Qiu et al (2013), describes further tests that can distinguish between partial and complete sex linkage based on population genetic evidence.…”

Section: Linkage Analysismentioning

confidence: 99%

“…the existence of a paralogous copy of E284; see the accompanying article in this issue, Qiu et al 2013), and they indicate linkage to the sex-determining region of the sex chromosomes and/or to other X-linked or PAR genes (Table 3 shows recombination distances in various families). For gene E200, partial sex linkage is well supported by recombinants in three different families (with small estimated recombination fractions with the X or Y PAR boundary).…”

Section: Genetic Map Of S Latifoliamentioning

confidence: 99%

“…Comparing the X chromosome genes and their genetic map with the map locations of their S. vulgaris orthologues reveals that chromosome regions have been added to the S. latifolia sex chromosomes to form the PAR region and that some of these genes have become fully sex-linked, suggesting recent formation of a new evolutionary stratum. In the accompanying article in this issue, Qiu et al (2013), we describe population genetic data that confirm the PAR locations of the PAR genes inferred by genetic mapping, and we use these genes in tests for sexual antagonism that employ sequence analyses.…”

mentioning

confidence: 99%

“…Such a polymorphic situation selects for reduced recombination with the fully sex-linked (sex-determining) region, because this increases transmission of the male-benefit allele to males and reduces transmission of these alleles to females (Charlesworth and Charlesworth 1980;Rice 1987;Mank and Ellegren 2009;Jordan and Charlesworth 2012). However, alternatives exist [see Discussion in the accompanying article in this issue (Qiu et al 2013)], and, no direct evidence currently connects SA alleles to the evolution of reduced recombination of Y or W sex chromosomes.…”

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confidence: 99%

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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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122

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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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“…The accompanying article in this issue, Qiu et al (2013), describes further tests that can distinguish between partial and complete sex linkage based on population genetic evidence.…”

Section: Linkage Analysismentioning

confidence: 99%

Section: Genetic Map Of S Latifoliamentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

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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122

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“…Most plants with separate sexes, however, appear to possess genetic s.d., with either heteromorphic or homomorphic sex chromosomes (Ming et al, 2011). Species with heteromorphic sex chromosomes include both those with an XY (for example, Cycas revoluta- (Segawa et al, 1971;Hizume et al, 1998); Cannabis sativa- (Sakamoto et al, 1998;Rode et al, 2005;Sakamoto et al, 2005); Silene latifolia- (Correns, 1928;Westergaard, 1958;Filatov, 2005;Nicolas et al, 2005;Marais et al, 2008;Qiu et al, 2013) and S. diclinis- Howell et al, 2009) or ZW s.d. (for example, Gingko biloba- (Lan et al, 2008); S. otitis- (Slancarova et al, 2013)).…”

Section: Introductionmentioning

confidence: 99%

Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives

Russell

Pannell

2014

Heredity

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Separate sexes have evolved on numerous independent occasions from hermaphroditic ancestors in flowering plants. The mechanisms of sex determination is known for only a handful of such species, but, in those that have been investigated, it usually involves alleles segregating at a single locus, sometimes on heteromorphic sex chromosomes. In the genus Mercurialis, transitions between combined (hermaphroditism) and separate sexes (dioecy or androdioecy, where males co-occur with hermaphrodites rather than females) have occurred more than once in association with hybridisation and shifts in ploidy. Previous work has pointed to an unusual 3-locus system of sex determination in dioecious populations. Here, we use crosses and genotyping for a sex-linked marker to reject this model: sex in diploid dioecious M. annua is determined at a single locus with a dominant male-determining allele (an XY system). We also crossed individuals among lineages of Mercurialis that differ in their ploidy and sexual system to ascertain the extent to which the same sex-determination system has been conserved following genome duplication, hybridisation and transitions between dioecy and hermaphroditism. Our results indicate that the maledetermining element is fully capable of determining gender in the progeny of hybrids between different lineages. Specifically, males crossed with females or hermaphrodites always generate 1:1 male:female or male:hermaphrodite sex ratios, respectively, regardless of the ploidy levels involved (diploid, tetraploid or hexaploid). Our results throw further light on the genetics of the remarkable variation in sexual systems in the genus Mercurialis. They also illustrate the almost identical expression of sexdetermining alleles in terms of sexual phenotypes across multiple divergent backgrounds, including those that have lost separate sexes altogether.

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Sex‐linked gene expression and the emergence of hermaphrodites in Carica papaya

Chae

Harkess

Moore

2021

American J of Botany

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Premise One evolutionary path from hermaphroditism to dioecy is via a gynodioecious intermediate. The evolution of dioecy may also coincide with the formation of sex chromosomes that possess sex‐determining loci that are physically linked in a region of suppressed recombination. Dioecious papaya (Carica papaya) has an XY chromosome system, where the presence of a Y chromosome determines maleness. However, in cultivation, papaya is gynodioecious, due to the conversion of the male Y chromosome to a hermaphroditic Yh chromosome during its domestication. Methods We investigated gene expression linked to the X, Y, and Yh chromosomes at different floral developmental stages to identify differentially expressed genes that may be involved in the sexual transition of males to hermaphrodites. Results We identified 309 sex‐biased genes found on the sex chromosomes, most of which are found in the pseudoautosomal regions. Female (XX) expression in the sex‐determining region was almost double that of X‐linked expression in males (XY) and hermaphrodites (XYh), which rules out dosage compensation for most sex‐linked genes; although, an analysis of hemizygous X‐linked loci found evidence of partial dosage compensation. Furthermore, we identified a candidate gene associated with sex determination and the transition to hermaphroditism, a homolog of the MADS‐box protein SHORT VEGETATIVE PHASE. Conclusions We identified a pattern of partial dosage compensation for hemizygous genes located in the papaya sex‐determining region. Furthermore, we propose that loss‐of‐expression of the Y‐linked SHORT VEGETATIVE PHASE homolog facilitated the transition from males to hermaphrodites in papaya.

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Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Cited by 55 publications

References 77 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

Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives

Sex‐linked gene expression and the emergence of hermaphrodites in Carica papaya

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