scholarly journals Chromosome-scale assembly of the genome of Salix dunnii reveals a male-heterogametic sex determination system on chromosome 7

2020 ◽  
Author(s):  
Li He ◽  
Kai-Hua Jia ◽  
Ren-Gang Zhang ◽  
Yuan Wang ◽  
Tian-Le Shi ◽  
...  

AbstractSex determination systems in plants can involve either female or male heterogamety (ZW or XY, respectively). Here we used Illumina short reads, Oxford Nanopore Technologies (ONT) long reads, and Hi-C reads to assemble the first chromosome-scale genome of a female willow tree (Salix dunnii), and to predict genes using transcriptome sequences and available databases. The final genome sequence of 328 Mb in total was assembled in 29 contigs, and includes 31,501 genes. We inferred a male heterogametic sex determining factor on chromosome 7, suggesting that, unlike the female heterogamety of most species in the genus Salix, male heterogamety evolved in the subgenus Salix. The S. dunnii X-linked region occupies about 3.21 Mb of chromosome 7, and is probably in a pericentromeric region. Our data suggest that this region is enriched for transposable element insertions, and about one third of its 124 protein-coding genes were gained via duplications from other genome regions. We detect purifying selection on the genes that were ancestrally present in the region, though some have been lost. Transcriptome data from female and male individuals show more male- than female-biased genes in catkin and leaf tissues, and indicate enrichment for male-biased genes in the pseudo-autosomal regions. Our study provides valuable genomic resources for studying sex chromosome evolution in Salicaceae family.

2020 ◽  
Vol 37 (8) ◽  
pp. 2357-2368 ◽  
Author(s):  
Yiyuan Li ◽  
Bo Zhang ◽  
Nancy A Moran

Abstract Different evolutionary forces shape gene content and sequence evolution on autosomes versus sex chromosomes. Location on a sex chromosome can favor male-beneficial or female-beneficial mutations depending on the sex determination system and selective pressure on different sexual morphs. An X0 sex determination can lead to autosomal enrichment of male-biased genes, as observed in some hemipteran insect species. Aphids share X0 sex determination; however, models predict the opposite pattern, due to their unusual life cycles, which alternate between all-female asexual generations and a single sexual generation. Predictions include enrichment of female-biased genes on autosomes and of male-biased genes on the X, in contrast to expectations for obligately sexual species. Robust tests of these models require chromosome-level genome assemblies for aphids and related hemipterans with X0 sex determination and obligate sexual reproduction. In this study, we built the first chromosome-level assembly of a psyllid, an aphid relative with X0 sex determination and obligate sexuality, and compared it with recently resolved chromosome-level assemblies of aphid genomes. Aphid and psyllid X chromosomes differ strikingly. In aphids, female-biased genes are strongly enriched on autosomes and male-biased genes are enriched on the X. In psyllids, male-biased genes are enriched on autosomes. Furthermore, functionally important gene categories of aphids are enriched on autosomes. Aphid X-linked genes and male-biased genes are under relaxed purifying selection, but gene content and order on the X is highly conserved, possibly reflecting constraints imposed by unique chromosomal mechanisms associated with the unusual aphid life cycle.


Genes ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 483
Author(s):  
Wen-Juan Ma ◽  
Paris Veltsos

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.


2021 ◽  
Vol 376 (1832) ◽  
pp. 20200089
Author(s):  
Heiner Kuhl ◽  
Yann Guiguen ◽  
Christin Höhne ◽  
Eva Kreuz ◽  
Kang Du ◽  
...  

Several hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet ( Acipenser ruthenus ). Using chromosome-scale assemblies and pool-sequencing, we first identified an approximately 16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages ( A. sturio, A. oxyrinchus versus A. ruthenus, Huso huso ), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species ( A. gueldenstaedtii, A. baerii ). Conservation of a female-specific sequence for a long period, representing 180 Myr of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.


2021 ◽  
Author(s):  
Anne-Laure Ferchaud ◽  
Claire Merot ◽  
Eric Normandeau ◽  
Ioannis Ragoussis ◽  
Charles Babin ◽  
...  

Despite the commercial importance of Greenland Halibut (Reinhardtius hippoglossoides), important gaps still persist in our knowledge of this species, including its reproductive biology and sex determination mechanism. In this study, we combined single molecule sequencing of long reads (Pacific Sciences) with Chromatin Conformation Capture sequencing (Hi-C) data to provide the first chromosome-level genome reference for this species. The high-quality assembly encompassed more than 598 Megabases (Mb) assigned to 1 594 scaffolds (scaffold N50 = 25 Mb) with 96 % of its total length distributed among 24 chromosomes. The investigation of its syntenic relationships with other economically important flatfish species revealed a high conservation of synteny blocks among members of this phylogenetic clade. Sex determination analysis revealed that flatfishes do not escape the rule applied to other teleost fish and exhibit a high level of plasticity and turnover in sex-determination mechanisms. A whole-genome sequence analysis of 198 individuals allowed us to draw a full picture of the molecular sex determination (SD) system for Greenland Halibut, revealing that this species possesses a very nascent male heterogametic XY system, with a putative major effect of the sox2 gene, also described as the main SD driver in two other flatfishes. Interestingly, our study also suggested for the first time in flatfishes that a putative Y-autosomal fusion could be associated with a reduction of recombination typical of early steps of sex chromosome evolution.


Author(s):  
Anne-Laure Ferchaud ◽  
Claire Mérot ◽  
Eric Normandeau ◽  
Jiannis Ragoussis ◽  
Charles Babin ◽  
...  

Abstract Despite the commercial importance of Greenland Halibut (Reinhardtius hippoglossoides), important gaps still persist in our knowledge of this species, including its reproductive biology and sex determination mechanism. Here, we combined single-molecule sequencing of long reads (Pacific Sciences) with chromatin conformation capture sequencing (Hi-C) data to assemble the first chromosome-level reference genome for this species. The high-quality assembly encompassed more than 598 Megabases (Mb) assigned to 1 594 scaffolds (scaffold N50 = 25 Mb) with 96% of its total length distributed among 24 chromosomes. Investigation of the syntenic relationship with other economically important flatfish species revealed a high conservation of synteny blocks among members of this phylogenetic clade. Sex determination analysis revealed that, similar to other teleost fishes, flatfishes also exhibit a high level of plasticity and turnover in sex-determination mechanisms. A low-coverage whole-genome sequence analysis of 198 individuals revealed that Greenland Halibut possesses a male heterogametic XY system and several putative candidate genes implied in the sex determination of this species. Our study also suggests for the first time in flatfishes that a putative Y-autosomal fusion could be associated with a reduction of recombination typical of the early steps of sex chromosome evolution.


2018 ◽  
Author(s):  
Peta Hill ◽  
Christopher P. Burridge ◽  
Tariq Ezaz ◽  
Erik Wapstra

AbstractSex determination systems are exceptionally diverse and have undergone multiple and independent evolutionary transitions among species, particularly reptiles. However, the mechanisms underlying these transitions have not been established. Here we tested for differences in sex-linked markers in the only known reptile that is polymorphic for sex determination system, the spotted snow skink, Niveoscincus ocellatus, to quantify the genomic differences that have accompanied this transition. In a highland population, sex is determined genetically, whilst in a lowland population, offspring sex ratio is influenced by temperature. We found a similar number of sex-linked loci in each population, including shared loci, with genotypes consistent with male heterogamety (XY). However, population-specific linkage disequilibrium suggests greater divergence of sex chromosomes in the highland population. Our results suggest that transitions between sex determination systems (GSD and TSD-like systems) can be facilitated by subtle genetic differences.


2019 ◽  
Author(s):  
Qiaowei Pan ◽  
Romain Feron ◽  
Ayaka Yano ◽  
René Guyomard ◽  
Elodie Jouanno ◽  
...  

AbstractTeleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes and the MSD genes they harbor is rather unexplored. We characterized a male-specific duplicate of the anti-Müllerian hormone (amh) as the MSD gene in Northern Pike (Esox lucius), using genomic and expression evidences as well as by loss-of-function and gain-of-function experiments. Using RAD-Sequencing from a family panel, we identified Linkage Group (LG) 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. Furthermore, we demonstrated that this MSD originated from an ancient duplication of the autosomal amh gene, which was subsequently translocated to LG24. Using sex-specific pooled genome sequencing and a new male genome sequence assembled using Nanopore long reads, we also characterized the differentiation of the X and Y chromosomes, revealing a small male-specific insertion containing the MSD gene and a limited region with reduced recombination. Our study depicts an unexpected level of limited differentiation within a pair of sex chromosomes harboring an old MSD gene in a wild population of teleost fish, highlights the pivotal role of genes from the amh pathway in sex determination, as well as the importance of gene duplication as a mechanism driving the turnover of sex chromosomes in this clade.Author SummaryIn stark contrast to mammals and birds, teleosts have predominantly homomorphic sex chromosomes and display a high diversity of sex determining genes. Yet, population level knowledge of both the sex chromosome and the master sex determining gene is only available for the Japanese medaka, a model species. Here we identified and provided functional proofs of an old duplicate of anti-Müllerian hormone (Amh), a member of the Tgf-β family, as the male master sex determining gene in the Northern pike, Esox lucius. We found that this duplicate, named amhby (Y-chromosome-specific anti-Müllerian hormone paralog b), was translocated to the sub-telomeric region of the new sex chromosome, and now amhby shows strong sequence divergence as well as substantial expression pattern differences from its autosomal paralog, amha. We assembled a male genome sequence using Nanopore long reads and identified a restricted region of differentiation within the sex chromosome pair in a wild population. Our results provide insight on the conserved players in sex determination pathways, the mechanisms of sex chromosome turnover, and the diversity of levels of differentiation between homomorphic sex chromosomes in teleosts.


Genes ◽  
2020 ◽  
Vol 11 (4) ◽  
pp. 374 ◽  
Author(s):  
Svetlana A. Romanenko ◽  
Antonina V. Smorkatcheva ◽  
Yulia M. Kovalskaya ◽  
Dmitry Yu. Prokopov ◽  
Natalya A. Lemskaya ◽  
...  

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.


2008 ◽  
Vol 4 (6) ◽  
pp. 700-703 ◽  
Author(s):  
Avner Cnaani ◽  
Thomas D Kocher

Cichlid species of the genus Oreochromis vary in their genetic sex-determination systems. In this study, we used microsatellite DNA markers to characterize the sex-determination system in Oreochromis tanganicae . Markers on linkage group 3 were associated with phenotypic sex, with an inheritance pattern typical of a female heterogametic species (WZ–ZZ). Further, locus duplication was observed for two separate microsatellite markers on the sex chromosome. These results further advance our understanding of the rapidly evolving sex-determination systems among these closely related tilapia species.


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