Next Generation Sequencing-Based Analysis of Repetitive DNA in the Model Dioceous Plant Silene latifolia

The existence of sexually antagonistic (SA) polymorphism is widely considered the most likely explanation for the evolution of suppressed recombination of sex chromosome pairs. This explanation is largely untested empirically, and no such polymorphisms have been identified, other than in fish, where no evidence directly implicates these genes in events causing loss of recombination. We tested for the presence of loci with SA polymorphism in the plant Silene latifolia, which is dioecious (with separate male and female individuals) and has a pair of highly heteromorphic sex chromosomes, with XY males. Suppressed recombination between much of the Y and X sex chromosomes evolved in several steps, and the results in Bergero et al. (2013) show that it is still ongoing in the recombining or pseudoautosomal, regions (PARs) of these chromosomes. We used molecular evolutionary approaches to test for the footprints of SA polymorphisms, based on sequence diversity levels in S. latifolia PAR genes identified by genetic mapping. Nucleotide diversity is high for at least four of six PAR genes identified, and our data suggest the existence of polymorphisms maintained by balancing selection in this genome region, since molecular evolutionary (HKA) tests exclude an elevated mutation rate, and other tests also suggest balancing selection. The presence of sexually antagonistic alleles at a locus or loci in the PAR is suggested by the very different X and Y chromosome allele frequencies for at least one PAR gene.

Section: Alternatives To Sa Selectionmentioning

confidence: 99%

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

Qiu¹,

Bergero²,

Charlesworth

2013

“…Although whole-genome sequencing can identify many genes and locate them on chromosomes, it is impractical for S. latifolia, due to its large genome size of almost 3 Gb (Costich et al 1991;Siroky et al 2001;Meagher et al 2005) and highly repetitive sequence content (Hobza et al 2007;Cermak et al 2008;Macas et al 2008). Moreover, sequencing alone does not identify the nonrecombining regions of the sex chromosomes.…”

mentioning

confidence: 99%

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

Bergero

Qiu

Forrest³

et al. 2013

122

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

“…Thus, it is unclear whether heteromorphic chromosomes have already developed in these species, such as asparagus (Asparagus officinalis) (Telgmann-Rauber et al 2007), Populus (Populus trichocarpa) (Yin et al 2008), and spinach (Spinacia oleracea) (Yamamoto et al 2014). Heteromorphic sex chromosomes were revealed cytologically in several plant species (Yamato et al 2007;Zhang et al 2008;Sousa et al 2013), including, Silene latifolia, which is one of the best-studied model plant species with well-differentiated X/Y chromosomes (Vyskot and Hobza 2004;Macas et al 2011). Multiple sex chromosomes, such as XY 1 Y 2 , were also reported in several plant species (Hizume et al 1988;Howell et al 2009;Mariotti et al 2009;Navajas-Perez et al 2009).…”

mentioning

confidence: 99%

Evidence for Emergence of Sex-Determining Gene(s) in a Centromeric Region in Vasconcellea parviflora

Iovene

Ming

et al. 2014

Sex chromosomes have been studied in many plant and animal species. However, few species are suitable as models to study the evolutionary histories of sex chromosomes. We previously demonstrated that papaya (Carica papaya) (2n = 2x = 18), a fruit tree in the family Caricaceae, contains recently emerged but cytologically heteromorphic X/Y chromosomes. We have been intrigued by the possible presence and evolution of sex chromosomes in other dioecious Caricaceae species. We selected a set of 22 bacterial artificial chromosome (BAC) clones that are distributed along the papaya X/Y chromosomes. These BACs were mapped to the meiotic pachytene chromosomes of Vasconcellea parviflora (2n = 2x = 18), a species that diverged from papaya 27 million years ago. We demonstrate that V. parviflora contains a pair of heteromorphic X/Y chromosomes that are homologous to the papaya X/Y chromosomes. The comparative mapping results revealed that the male-specific regions of the Y chromosomes (MSYs) probably initiated near the centromere of the Y chromosomes in both species. The two MSYs, however, shared only a small chromosomal domain near the centromere in otherwise rearranged chromosomes. The V. parviflora MSY expanded toward the short arm of the chromosome, whereas the papaya MSY expanded in the opposite direction. Most BACs mapped to papaya MSY were not located in V. parviflora MSY, revealing different DNA compositions in the two MSYs. These results suggest that mutation of gene(s) in the centromeric region may have triggered sex chromosome evolution in these plant species.KEYWORDS FISH; centromere; heterochromatin; sex chromosome H ETEROMORPHIC sex chromosomes (X/Y, Z/W) evolved from pairs of autosomes (Ming et al. 2011;Bachtrog 2013;Charlesworth 2013). It is generally accepted that sex chromosome evolution is initiated by the emergence of a sexdetermining locus. Suppression of recombination surrounding the sex-determining locus, which favored the linkage of the sex-determining alleles with sexually antagonistic alleles, caused the decay of the Y/W chromosomes and resulted in a pair of heteromorphic sex chromosomes (Ming et al. 2011;Bachtrog 2013;Charlesworth 2013). Sex chromosomes evolved independently in different eukaryotic lineages. The mammalian X chromosome and the bird Z chromosome evolved from different portions of the ancestral genome (Bellott et al. 2010;Cortez et al. 2014). Interestingly, all therian mammals have homologous XY systems and all birds have homologous ZW systems (Graves 2008). Thus, these sex chromosomes, surprisingly, appear to have evolved only once in each of these two major evolutionary clades.Compared to mammals and birds, sex chromosomes have emerged more frequently in several other eukaryotic lineages, including plants. Sex chromosomes have been reported in at least 48 plant species across 20 different families, including both X/Y and Z/W systems (Ming et al. 2011;Kumar et al. 2014). Sex chromosomes in some plant species were identified using genetic mapping-based approaches. However, cyto...