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Teleost 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.
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 LG X-master 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 reveals an unexpectedly low level of differentiation between a pair of sex chromosomes harboring an old MSD gene in a wild teleost fish population, and highlights both 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.
In stark contrast to mammals and birds, a high proportion of teleosts have 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. 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.
PLoS Genet 15 8 : x-master This is an open access article distributed under the terms of the Creative Commons Attribution Licensewhich permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. The evolution of x-master determination SD systems and sex chromosomes has sparked the interest of evolutionary biologists for decades.
X-master initial insights on sex chromosome evolution came from detailed studies in Drosophila and in mammals [ 1 — 5 ], recent research on other vertebrate groups, such as avian [ 67 ], non-avian reptiles [ 89 ], amphibians [ 10 — 13 ], and teleost fishes [ 14 — 17 ], has provided new information that helps us understand the evolution of SD systems and sex chromosomes.
Teleosts display the highest diversity of genetic sex determination systems in vertebrates, including several types of monofactorial and polygenic systems [ 1418 ]. In addition, in some species, genetic factors can interact with environmental factors, most commonly temperature, i. Moreover, sex determination systems in fish can differ between very closely related species, as illustrated by the group of Asian ricefish genus Oryzias [ 20 — 25 ], and sometimes even among different populations of one species, as in the Southern platyfish, Sex maculatus [ 26 ].
Beside this remarkable dynamic of sex determination systems, the rapid turnover of sex chromosomes in teleosts provides many opportunities to examine sex chromosome pairs at different stages of differentiation.
Finally, recent studies on fish sex determination have revealed a dozen new master sex determining MSD genes [ 141627 ], providing additional insight to the forces driving the turnover of SD systems and the formation of sex chromosomes. The origin of new MSDs falls into two categories: either gene duplication followed by sub- or neo-functionalization, or allelic diversification [ 14 ].
To date, teleosts are the only group where examples of both gene duplication and allelic diversification mechanisms have been found [ 14 — 17 ].
Furthermore, the duplicated MSD gene could potentially be inserted into different chromosomes and thus provide further flexibility in sex chromosome turnover. To understand how the mechanism of MSD origin could impact the evolution of sex chromosomes, additional empirical studies identifying the origin of MSDs and sex chromosomes are urgently needed.
Such studies will form a rich knowledge base allowing advances of theories of sex chromosome evolution. Among identified teleost MSD genes, the salmonid MSD gene, named sdYis the most intriguing because it revealed a previously unexpected flexibility in SD pathways in teleosts. The first step to answer this question was to identify the genetic component responsible for sex determination in E. It has emerged as an important model species for ecology and conservation because of its pivotal role as a top predator that shapes the structure of local fish communities, and sex as a valuable food and sport fish [ 36 ].
Consequently, genomic resources have recently been generated for E. Yet, little is known about genetic sex determination in E.
Using pooled sequencing pool-seq reads from a wild population and a new draft genome sequenced with Nanopore long reads, we found limited differentiation between the homomorphic sex chromosomes and that this male-specific duplicate of amhwhich we call amhbyis located within the Y-specific sequence.
Using RAD-sequencing of a family panel, we identified Linkage Group 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. In addition, we showed that amhby has an expression profile characteristic of a male MSD gene and x-master functionally both sufficient and necessary to trigger testis development, providing robust support for amhby as the MSD gene in this species. Finally, through phylogenetic and synteny analyses, we showed that this amh duplication occurred around 40 million years ago and that amhby was translocated after its duplication, which likely initiated the formation of the proto-Y chromosome.
Taking advantage of recent advances in functional genomics and sequencing technologies, our study combines the location and characterization of the sex locus and the identification of a master sex determining MSD gene with substantial functional validation in a non-model species.
Our results expand the knowledge of sex determination genes and provide insight on the evolution of sex chromosomes in teleosts. By searching tissue-specific transcriptomes of E. The two amh transcripts share Each lane corresponds to one individual.
The number of tested animals of each sex positive for amha and amhby is indicated in the table on the right. B Sequence identity of global pairwise alignment between amha and amhby genomic sequences with the amhby sequence as reference. C Schematic representation of amha and amhby gene structure in E. Exon1-Exon7 are represented by green boxes with shared percentage identity indicated and introns are represented by white segments.
The red segment in intron 1 represents the amhby specific insertion. D Global pairwise alignment between 5 kb upstream region of amha and amhby with amhby as the reference.
The start codon of each gene is positioned at 0 bp and the number on the y-axis indicates distance from the start codon upstream to the coding sequence. To compare the genomic regions containing amha and amhbyclones were isolated from a phenotypic male genomic fosmid library and sequenced. Predicted proteins contain amino-acids AA for amha and AA for amhbysharing To identify the sex chromosome in the genome of E.
Genome-wide average F ST between male and female offspring was 0. Furthermore, only markers mapped to LG24 showed genome-wide association with sex phenotype Fig 2Aindicating that LG24 is the sex chromosome of E.
Linkage group 24 showed sex concentration of markers significantly associated with sex phenotype. Recombination is observed along the entire length of LG24 in females and for most male markers except a group aligned to a region between 1. Black dotted-line box highlights the group of male markers that shows no recombination with the sex locus with a zoomed-in view on the side.
C : Number of male and female-specific SNPs from pool-seq in 50 kb sex windows is plotted along LG 24 with zoomed-in view on the first 1Mb. The male data are represented in blue and female in red. To locate the sex locus and to investigate the pattern of recombination between sex X and Y chromosomes in the paternal genome, we compared LG24 in the male and female RAD-Seq genetic maps.
In the female map, recombination was observed along the entire length of LG In the male map, while recombination with the sex locus 0 cM in the genetic x-master was observed for the majority of the LG24 markers, 11 markers aligned to a small kb region between 1. Additionally, 20 markers showed no recombination with the sex locus and could not be aligned to the female reference genome, suggesting that they are Y-specific sequences.
Two of these 20 markers aligned to the amhby sequence, indicating that amhby is passed down strictly from father to sons S3 Table. Furthermore, in a separate analysis, we identified the parental origin of all markers and plotted the distribution of these markers between male and female offspring along LG24 S5 Fig.
While maternal markers showed no sex bias in their distribution among offspring, paternal markers displayed an important sex-bias at the proximal end of LG24, again locating the sex locus to this region. This recombination pattern of RAD-Seq markers aligned to LG24 inferred from a single family panel represents the X and Y recombination pattern of the sire.
In order to characterize the differentiation between the X and Y chromosomes at the population level, we sequenced a pool of 30 phenotypic males and a pool of 30 phenotypic females. The genome average was 0. A sex analysis with a higher 2. These results confirm that the sex locus is located in the proximal of LG24, and indicate that at the population level, there is strong differentiation between the X and the Y sequences restricted to a small kb sub-telomeric region of the LG24 sex chromosome.
Therefore, to better characterize the Northern pike sex locus, we sequenced and assembled the genome of a genetic male with Nanopore long reads. In this Nanopore assembly, the entire sequence of the amhby -containing fosmid was included in a 99 kb scaffold tigfrom 24, bp x-master 60, bp, with amhby located from 27, bp to 30, bp.
To identify these potential Y-specific sequences absent in XX females, we aligned the pool-seq reads to the XY Nanopore assembly and searched for non-overlapping 1 kb regions covered only by male reads MR1k. Blasting results on the three MR1k-containing Nanopore contigs showed that amhby is the only protein coding gene apart from transposable elements TEs associated sex in the E. To quantify the length of Y-specific sequences, we then looked for regions with few or no female reads mapped and male reads mapped at a depth close to half of the genome average on the three MR1k-containing contigs from the Nanopore assembly S6 Fig.
Together, these results indicate that the size of the sex locus of E. To characterize the temporal and spatial expression of amhby in relation to the molecular and morphological differentiation between male and female gonads, both quantitative PCR qPCR and in-situ hybridization ISH were performed. Expression of amhbyamhathree other genes drmt1cyp19a1aand gsdf known for their role in gonadal sex differentiation, and amhrIIthe putative receptor for the canonical amhwas measured by qPCR at four time points from 54 days post-fertilization dpf to dpf, prior to the onset of gametogenesis.
The entire trunks were used for the first three time points when the gonads were too small to be isolated, and only gonads were used at dpf for both males and females. Expression of drmt1cyp19a1aand gsdf was only detected from dpf onwards, i. Expression of amhrII was not detected until dpf and did not differ significantly between sexes at any stage S7 Fig.
A-B : Boxplots showing the first quantile, median, and the third quantile of the temporal expression of A amha and B amhby during early development of E.
Outliers are displayed as dots. The mRNA expression of amha and amhby was measured at 54, 75,and days post fertilization dpf in male and female samples of E. Statistical tests were not performed on amhby expression between sexes because of the complete absence of x-master expression in females. C-F : In situ hybridization on histological sections revealed the localization of amha in both 80 dpf C female and D male gonads, with a stronger expression in male gonads.
A high amhby mRNA expression is detected in the male x-master Fwith no signal detected in female gonad E. Expression of amha and amhby was also characterized by in-situ hybridization ISH performed on histological sections of the entire trunk of male and female E. Expression of amha was detected in the gonads of both female Fig 3C and male Fig 3D samples, but the signal was much stronger in male gonads.
In contrast, expression of amhby was strong in male gonads Fig 3F but not detected in female gonads Fig 3Econfirming the specificity of the probe for amhby. In addition, no morphological differences were observed between sex and female gonads at 80 dpf, even though expression of amhby was already detected by qPCR and by ISH at this stage.
Our ISH results show that the expression of both amha and amhby is high in male gonads before the first signs of histological differentiation between male and female gonads. Collectively, these results show that amhby is expressed in the male gonads prior to both molecular and morphological sexual-dimorphic differentiation of gonads in E. Sex further investigate the functional role of amhby in initiating testicular development, we performed both loss-of-function and gain-of-function experiments.
Overall, 12 of 36 G1 XY offspring obtained from three amhby mosaic G0 males crossed with wild-type females were maintained until the beginning of testicular gametogenesis at dpf and then processed sex histology.
Control animals developed normal ovaries and testes Fig 4A and 4Bbut all 23 XY F1 amhby mutants failed to develop a normal testes. The amhby X-master XY individual C developed ovaries with oocytes and an ovary cavity, indistinguishable from the ovary of the control females A. The amhby transgenic XX mutant individual D developed testis with clusters of spermatozoids and testicular lobules identical to that of the control males B.
To investigate whether amhby alone is sufficient to trigger testicular development, we overexpressed amhby in XX genetic females.
Creator: Michelle Ashford. Added to Watchlist. Top-Rated Episodes S4. Error: please try again. Emmys Trending Widget Titles. Tv Shows Need to Finish. TV series I've seen. TV Shows - end. How Much Have You Seen? How many episodes of Masters of Sex have you seen? Share this Rating Title: Masters of Sex — 7. Use the HTML below. You must be a registered user to use the IMDb rating plugin.
User Polls Sex and the TV Episodes Seasons. Nominated for 2 Golden Globes. Learn more More Like This. Californication — Comedy Drama. Kenneth Williams: Fantabulosa! TV Movie Biography Comedy Drama. Girls — A comedy about the experiences of a group of girls in their early 20s. Sex and the City — Comedy Drama Romance.
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Edit Cast Series cast summary: Michael Sheen William Masters 46 episodes, Lizzy Caplan Virginia Johnson 46 episodes, Caitlin FitzGerald Libby Masters 46 episodes, Annaleigh Ashford Betty DiMello 37 episodes, Teddy Sears Austin Langham 29 episodes, Kevin Christy Lester Linden 26 episodes, Beau Bridges Edit Storyline Dr.
Country: USA. Language: English. Runtime: 60 min. Sound Mix: Dolby Digital. Color: Color. Edit Did You Know? This building had previously been used for exteriors of Blair General Hospital in the "Dr.
Kildare" movies and TV series. Goofs In the introduction sequence, the quarter being inserted into the vending machine behind Michael Sheen's name says, "Quarter Dollar" under Washington's profile.
This design was introduced for the "50 State Quarters" program, which began in A quarter from the time of this show, set more than 40 years earlier than this TV show, would clearly show the year of minting beneath Washington's profile.
Add the first question. Was this review helpful to you? Yes No Report this. So they used a variety of different instruments.
One of the instruments that they used was to trace the breathing and the heart rates and such. It was also used to internally observe sexual response by women, and that had a nickname called 'Ulysses. In other words, they were all aware that there had never been a study of human beings. They had studied rabbits; they had studied apes. And in fact, that's kind of how Bill Masters, studying anatomy both in Rochester and later at Johns Hopkins, became aware that this was something that had never been done.
He traveled in the circle of doctors that were looking to win the Nobel Prize for And he felt, though, that this Your purchase helps support NPR programming. Masters and Johnson really underlined the power of female sexuality, and in their long-term study what they showed was that women had the capacity for multiple orgasms in a way that men would go into what they called 'a refractory period' after having the initial sexual orgasm.
Women were capable of multiple orgasms, and the second and the third was more intense than the first, and And this was something that was done with about women, almost an equal number of men, and they recorded something like 10, orgasms over a decade-long study that formulated their major book, Human Sexual Response , that came out in Louis, where he was in many ways the best doctor in St.
He had a lot of rich clients. He was very aware that the experience[s] of prostitutes were different than everyday women. One of the things that I found in doing research was I found the police commissioner in St. Louis, a guy named Sam Priest. Priest when she delivered her babies.
So Sam Priest, the top cop in St. Louis, he loved Dr. Masters, he thought he was the greatest, the way that So whatever Masters wanted to do in that regard, [Priest] was more than willing to accommodate.
He asked about orgasm, and she said that she often faked orgasm. And he said, 'What do you mean "faking orgasm? And he seemed like he was struck by lightning, that the light bulb went off on his head. And it was the student On the researchers' use of sex surrogates, who are intimate with patients in order to achieve a therapeutic goal.
Medicine could deal with the various problems that couples had, individuals had. One of the problems was impotence for men, and they found that sex surrogates could be quite effective with men who were having problems performing. Bill Masters had a certain So he believed in sex surrogates. But what happened was that there were some legal consequences that came across there, and I think that Masters and Virginia [Johnson] So the lawsuit was quietly taken care of by their lawyers and they kind of vowed that Ultimately, it was too difficult; it was too hot to handle, frankly, politically.
It was always [a] problem for them that the subject of sex was something that medicine, they felt, should get involved in, but medicine wasn't really willing to do so.
Pairings and perspectives shift as the night wears on, until the light of day exposes the consequences of the Masters' big day is at hand after 12 months of studies. Without Virginia as a voice of moderation will Bill's pitch hit the mark?
Margaret Scully is confronted with her husbands homosexuality and Watch now. Title: Masters of Sex — A writer tries to juggle his career, his relationship with his daughter and his ex-girlfriend, as well as his appetite for beautiful women.
Martyn Hesford's comedy-drama about the life and times of tortured comic Kenneth Williams based on his diaries. Four female New Yorkers gossip about their sex lives or lack thereof and find new ways to deal with being a woman in the s. Inin Los Alamos, New Mexico, a team of government scientists is working on the top secret Manhattan Project in a race to produce an atomic bomb before the Nazis.
Meanwhile, their families adjust to a life on the military base. A struggling novelist and a young waitress sex up an extramarital relationship that promises to forever change the course of their lives. A tale of the bungling of Armageddon features an angel, a demon, an eleven-year-old Antichrist, and a doom-saying witch. The murder of a young boy in a small coastal town brings a media frenzy, which threatens to tear the community apart.
A drama about one of New York's most prestigious ad agencies at the beginning of the s, focusing on one of the firm's most mysterious but extremely talented ad executives, Donald Draper.
An adaptation of X-master Waugh's novel "Vile Bodies", is a look into the lives of a young novelist, his would-be lover, and a host of young people who beautified X-master in the s. Soon after local entrepreneur Ripley Holden Morrissey opens his arcade in his beloved home town of X-master, a murder investigation makes tears at the fabric of his x-master and professional lives. Fertility surgeon and specialist, Dr.
William Howell Masters, also fascinated with the science surrounding human sexuality, meets future research partner, Virginia Ellis Johnson, at Washington University in Missouri. Written by LA-Lawyer.
The title "Masters of Sex" works on many levels and the creators of the show are well aware of the attention that this title will draw. This show is about the x-master scientific research in the area of sex based on the Masters and Johnson studies, who are the sex of the story set to the backdrop of the late 's at Washington University in St.
Louis, Missouri. The set design is just about right and it very accurately represents the theme and ideology of the time. The characters are sketched out perfectly and x-master is no dearth of good acting performances with Michael Sheen stealing the sex for his portrayal of sex incredibly complex William Masters. The main part of the show is of course the study of human sexual response sex implies a lot of mature content.
Sex scenes, however tastefully done, may be a little too strong for the average viewer but if one can get x-master the explicit content, one x-master see their relevance to the plot. The story still seems a little empty at certain times but can be expected to fill up as it progresses with the introduction of new characters.
All in all, a very well presented and unique show. Start your free trial. Sign In. Keep track of everything you watch; tell your friends. Full Cast and Crew. Release Dates. Official Sites.
Company Credits. Technical Specs. Episode List. Plot Summary. Plot Keywords. Parents Guide. External Sites. User Reviews. User Ratings. External Reviews. Metacritic Reviews. Photo Gallery. Trailers and Videos. Crazy Credits. Alternate Versions. Rate This. Episode Guide. Drama about the pioneers of the science of human sexuality whose research touched off the sexual revolution. Creator: Sex Ashford. Added to Watchlist. Top-Rated Episodes S4. Error: please try again. Emmys Trending Widget Titles.
Tv Shows Need to Finish. TV series I've seen. TV Shows - end. How Much Have You Seen? How many episodes of Masters of Sex have you seen? Share this Rating Title: Masters of Sex — 7. Use the HTML below. You must be a registered user to use the IMDb rating plugin. User Polls Sex and the Sex Episodes Seasons. Nominated for 2 X-master Globes.
Learn more More Like This. Californication — Comedy Drama. Kenneth Williams: Fantabulosa! TV Movie Biography Comedy Drama. Girls — A sex about the experiences of a group of girls in their early 20s. Sex and the City — Comedy Drama Romance. Big Love — A polygamist and his relationship with his three wives. Manhattan — Drama History War. The Affair TV Series Good Omens Comedy Fantasy. Broadchurch — Crime Drama Mystery. Mad Men — Bright Young Things Comedy Drama War. Blackpool Comedy Crime Drama.
Edit Cast Series cast summary: Michael Sheen William Masters 46 episodes, Lizzy Caplan Virginia Johnson 46 episodes, Caitlin FitzGerald Libby Masters 46 episodes, Annaleigh Ashford Betty DiMello 37 episodes, Teddy Sears Austin Langham 29 episodes, Kevin Christy
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