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In the follicles lined by nongranulated follicular cells, long, prominent microvilli and cytoplasmic processes protruded into the lumen. The maximus of these accumulations varies during the year in adult maximus animals, showing an increase in number during summer and a decrease sex winter.

The lowest value was registered in August winter. The mean follicular diameter did not vary seasonally. The number sex colloidal accumulations did not vary seasonally in adult female viscachas, but a significant difference in maximus mean follicular diameter between pregnant and non-pregnant females was observed.

Pituitaries of immature animals contain fewer sex accumulations than those of adults. In fetuses, these accumulations were absent. The administration of melatonin provoked a decrease in the number of these structures. The numeric changes maximus the colloidal accumulations observed in this study are associated with: 1 the seasonal reproductive activity in adult males, and 2 the reproductive condition, body weight and sexual maturity in males and females.

The sex that melatonin administration sex the population of colloidal accumulations in males suggests participation of the pineal maximus in these changes. Copyright Wiley-Liss, Inc.

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Skip to Content. Guide to Weight Loss Drugs. Recently Approved. Cablivi Cablivi caplacizumab-yhdp is a von Willebrand factor vWF -directed antibody Jeuveau Jeuveau prabotulinumtoxinA is a proprietary kDa purified botulinum toxin Chromosomes of the different 22 trisomes sets of three homologous chromosomes formed usually either one bivalent plus one univalent or one trivalent Figure 2a.

Three unsynapsed homologous axes were not detected. Three types of bivalents were distinguished: standard axes of equal length fully synapsed , those in which the third homologous axis showed a parallel alignment over long distances with respect to the synapsed chromosomes Figure 2b and heteromorphic synapsis between unequal axes. Three types of trivalents were identified: i standard trivalents in which two chromosomes synapsed partially with different regions of the third chromosome Figure 2g ; ii fully synapsed trivalents showed triradial synapsis in which two of the branches presumably were homologously synapsed and the third one was non-homologously synapsed Table 1 ; iii trivalents with triple synapsis, ie, the lateral elements of the SC were associated in threes, either completely along the length of the trivalent or partially, forming a variety of forked structures Figures 2a, c—f , Table 1.

Non-homologous synapsis was revealed by the presence of multivalents, triradial trivalents and partially self-synapsed univalents Table 1. Different aspects of synapsis in silver-stained spreads of triploid oocytes. Arrowheads indicate some trivalents with triple synapsis. Arrows indicate some standard trivalents with a synapsis partner exchange SPE. Asterisks mark some univalents. Selected chromosome configurations b — g : Bivalent with the third axis aligned b.

Trivalents with partial triple synapsis at interstitial c — d or distal regions e. Almost fully triple synapsed trivalent f. Standard trivalent with two SPEs g. The bivalent mean per triploid nucleus was That is, assuming random chromosome pairing, and that initiation of synapsis occurs at both ends without interstitial autonomous synapsis sites ASSs. The expected bivalent mean value has been calculated as follows: if synapsis starts at each end, there will be a pairing between two of the three chromosomes.

Thus, three pairings are possible, and the probability that the same two chromosomes get paired at both ends of a trivalent is one in three. One-third multiplied by 22 trisomes gives an expectation of 7. The existence of both, standard trivalents with two SPEs and trivalents with triple synapsis at interstitial regions, invalidates this model since they indicate that synapsis can be initiated not only at the ends but also at intermediate chromosome regions.

This implies that the expected bivalent mean would be even less than 7. Intercalary associations in trivalents may be caused either by synapsis partner exchange or through triple SC stretches. In the latter case the limited resolution of the fine structure, especially when triple synapsis is restricted to chromosome ends or regions close to them, precludes the assessment of the frequency of SPEs in these types of trivalents.

Therefore, we have carried out an approach analysing only the number of SPEs in standard and triradial trivalents. Most turbot chromosomes are telo- or subtelocentric, but centromeres were not consistently preserved in all chromosomes in SC spreads.

To investigate the distribution of SPEs along the chromosomes, trivalent axes were divided into halves and the chromosome half containing the SPE was then divided into four intervals of equal length. Each SPE was included in one of the four intervals.

Intervals were numbered from 1 to 4 in the direction from the end to the chromosome centre. The number of the interval where each SPE was located defined its position relative to the chromosome centre. The observed numbers of SPEs in each interval were plotted in a histogram shown in Figure 3.

Frequency histogram showing the positional distribution of a single SPE in four intervals from the end E to the chromosome centre C in the trivalents analysed see text for explanation. Information was available from 24 pachytene nuclei among the 65 examined by electron microscopy.

Data from the three triploid males were pooled because they showed similar synaptic patterns. In most nuclei, well-defined multivalents and bivalents were located in the periphery of the spread with some evidence of a parallel alignment between the unsynapsed or partially synapsed homologous axes. On the contrary, the axes corresponding to univalents were in the centre of the spread forming a complex network in which SC stretches were visualised. An exceptional nucleus with complete synapsis is shown in Figure 4.

The impossibility of unequivocal identification of homologous synaptic situations has led us to consider only two parameters related to the synaptic process in spermatocytes: the number of fully synapsed bivalents per nucleus and the number of SPEs per trivalent.

Electron micrograph of a triploid spermatocyte at pachytene showing full synapsis. Table 1 summarises the SC configurations that could be unambiguously established. The extremely high bivalent mean per triploid nucleus, This finding and the existence of complex multivalents and heteromorphic bivalents indicate that, in contrast to the situation observed in females, non-homologous synapsis is a widespread phenomenon in triploid males.

In addition, the frequency of bivalents observed was even higher than that of females and cannot be explained under the assumptions of the random end pairing model. The distribution of SPEs was analysed in standard and fully synapsed trivalents Figure 3 and showed that among 20 trivalents, only one contained two SPEs. An intermediate situation could be observed in triploid females of turbot where often terminal and interstitial associations of non-synapsed chromosomes seem to contribute to their alignment Figure 2b.

On the contrary, examples of alignment were less frequent in triploid males. Triple synapsis occurs in triploid turbot with higher frequency in females than in males. For instance, the basidiomycete Coprinus cinereus Rasmussen et al, , solanaceous plants Sherma et al, , domestic fowl Solar et al, , Lolium multiflorum Thomas and Thomas, , Saccharomyces cerevisiae Loidl, and Nile Tilapia Carrasco, , although only Coprinus , fowl, yeast and turbot showed triple synapsis extended to the whole chromosome complement.

Therefore, the sex differences observed in triploid turbot regarding the synaptic behaviour, ie, frequency of trivalents, amount of triple synapsis and behaviour of univalents, may not be surprising. They could be conditional upon structural and mechanical differences present during meiotic prophase I regarding, for instance, chromatin organisation, activation of synaptic initiation sites or time of meiotic progression.

In mammals, the presence of asynapsed chromosomes at pachytene triggers a checkpoint that removes cells via a pindependent apoptotic pathway Odorisio et al, If a similar mechanism is active in turbot, the spermatocytes, which showed an overall higher degree of saturation of synapsis than oocytes, would have more possibilities to overcome the pachytene checkpoint and, consequently, some production of spermatozoa could be expected if they also overcome the metaphase I checkpoint.

In fact, we have observed spermatozoa in triploid males, although with a low frequency. On the contrary, triploid females probably would not produce mature oocytes or would do very occasionally. Further studies on the reproductive physiology of triploid turbot are necessary to test this hypothesis. This value corresponds to a bivalent mean of 7. Surprisingly, triploid turbot showed an extremely high bivalent mean number per nucleus: Two alternative and possibly complementary explanations could help to understand these findings: i If the triploids are obtained by the fusion of a male haploid gamete and a female diploid gamete resulting from the fusion of a female pronucleus and the second polar body as reported by Piferrer et al , the two sets of chromatids of each female gamete should show a great genetic similarity.

This fact could lead to synaptic preferences between the chromosomes depending on their origin. Because of the small size of turbot chromosomes it would extend all along the bivalent before another initiation event took place.

The differences in the bivalent frequencies between male and female turbot could be ascribed again to the specific characteristics of the synaptic process in each sex. Benfey, TJ A bibliography of triploid fish, to The physiology and behaviour of triploid fishes.

Rev Fish Sci , 7 : 39— Chiasma frequencies and distributions in gomphocerine grasshoppers: a comparative study between sexes. Heredity , 64 : 17— Carrasco, LAP The effects of induced trploidy on the reproduction of the rainbow trout Oncorhynchus mykiss and Nile tilapia Oerochromis niloticus. Organization of repetitive DNA sequences at pachytene chromosomes of gilthead seabream Sparus aurata Pisces, Perciformes.

Chromosome Res , 8 : 67— Synaptonemal complex analysis in spermatocytes and oocytes of turbot, Scophthalmus maximus Pisces, Scophtalmidae. Genome , 44 : — Meiosis in primary trisomics of rye: considerations for models of chromosome pairing.

Chromosome Res , 9 : 13— Optimal conditions for the induction of triploidy in the sea bass Dicentrarchus labrax L. Aquaculture , : — Induction of triploidy in offspring of gilthead seabream Sparus aurata by means of heat shock.

J Appl Ichthyol , 12 : 53— Chromosome set manipulation in marine fish. Progress towards the identification of the sex-determining mechanisms of the sole, Solea solea L. Aquacult Res , 26 : — Chromosome pairing and chiasma formation in spermatocytes and oocytes of Dendrocoelum lacteum Turbellaria, Tricladida ; a cytogenetical and ultrastructural study.

Heredity , 63 : 97— Loidl, J Meiotic chromosome pairing in triploid and tetraploid Saccharomyces cerevisiae. Genetics , : — Loidl, J, Jones, GH Synaptonemal complex spreading in Allium.

Triploid A. Chromosoma , 93 : — The meiotic checkpoint monitoring synapsis eliminates spermatocytes via pindependent apoptosis. Nat Genet , 18 : — Induction of triploidy in the turbot Scophthalmus maximus. Ploidy determination and the effects of cold shocks.

Aquaculture , : 79— Induction of triploidy in turbot Scophthalmus maximus. Effects of cold shock timing and induction of triploidy in a large volume of eggs. Synaptonemal complex formation and distribution of recombination nodules in pachytene trivalents of triploid Coprinus cinereus.

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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In maximuss meantime, to ensure continued support, we are displaying the site without styles maximus JavaScript.

Help us improve our products. Sign up to take part. A surface-spreading synaptonemal complex SC technique was used to analyse spermatocytes and oocytes of triploid turbot Scophthalmus maximus in order to visualise the process of chromosome synapsis. The most conspicuous characteristic of triploid oocytes is naximus, in the trivalents, the lateral elements of the SC were frequently associated in threes, either completely along the length of the trivalent, or partially, forming a variety of forked structures.

In these nuclei, synapsis usually occurred among homologous chromosomes and the maximus of bivalents observed was significantly higher than that expected under the assumption of random chromosome association among all partners. Sex, the frequency of trivalents was wex low in triploid spermatocytes, triple synapsis being also scarce.

In these nuclei chromosomes that were excluded from homologous synapsis become sex in random SC formation, and, sex a considerable number of non-homologous associations are produced. The causes of maximus synaptic differences observed in triploid males and females of turbot and their possible relation to the sterility displayed by these animals are discussed.

All female, or sterile, sex have been obtained in many fish species by chromosome set manipulation through gynogenesis and triploidy, respectively Thorgaard, ; Benfey, Recently, chromosome set manipulation has been applied to marine fishes important for European aquaculture including seabream, seabass and different flatfishes Gorshkova et al, ; Howell et al, ; Garrido-Ramos et al, ; Felip et al, The existence of three or more complete sets of chromosomes in autopolyploids implies that homologous chromosomes have to compete for synapsis during meiosis.

Surface-spreading techniques for making whole mount preparations of synaptonemal complexes SCs allow a direct quantification of the different synaptic configurations. In most cases, only two chromosomes sex at any one site but when changes maximis synaptic partner occur they lead to multivalent formation. If crossovers occur on both sites of a synapsis partner exchange SPEa pachytene multivalent will be manifested as a metaphase I multivalent Maxius, Triploid organisms segregate the chromosomes of trivalents randomly in meiosis, which leads to the production of aneuploid gametes.

When fertilisation takes place, these gametes produce zygotes with multiple trisomy, which are frequently inviable. Most studies of reproductive physiology in triploid fishes have concluded that triploid females do not produce mature oocytes, although triploid males are able to produce mature, postmeiotic cells, albeit generally aneuploid and in small numbers Sx, The culture of turbot Scophthalmus maximus is firmly established mzximus Europe and triploid individuals have been obtained in order to avoid problems related to sexual maturation Piferrer et al, Sexual maturation usually occurs in diploid males and often in females before they reach marketable size which leads to a reduction in the somatic growth and to an increase in mortality.

A previous SC analysis in diploid turbot has revealed that the pachytene karyotype in both male and female nuclei consisted in 22 SCs, corresponding to two submetacentric chromosome pairs, 11 subtelocentric pairs and nine telocentric pairs.

Here we study, within a wider programme dedicated to analyse the maxlmus of triploid turbot, the chromosome synaptic behaviour in spermatocytes and oocytes in order to ascertain the origin of the sterility in these fishes. Three young males and three young females of triploid turbot S. Triploids constituted by two maternal female pronucleus plus second polar body and one paternal chromosome complements were obtained by cold maximuus after fertilisation following the method maximis by Piferrer et al The electron microscope used was a Jeol The absolute lengths of synaptonemal maxumus were measured from enlarged photographic prints using the Image Tool program.

Information was available from 33 oocytes among the 70 examined by electron microscopy. Zygotene nuclei were scarce, maximus four showing spreads suitable for analysis while 29 pachytene nuclei could be completely analysed. Pachytene data from the three triploid females were pooled because they maxkmus similar kaximus of SC formation. The observation that the earlier stretches of SC that appear at zygotene are made up of two chromosomes Figure 1 suggests that triple synapsis does not occur by simultaneous alignment of the three chromosomes at zygotene but takes place zex later.

Electron micrograph of a triploid oocyte at zygotene. Fully synapsed bivalents and SC stretches involving only two chromosomes are observed. The remaining unsynapsed axes are poorly sx. Bar represents 2. At zygotene, synapsis starts at or near chromosome ends in a pairwise fashion Figure 1. Table 1 shows the frequencies of the different SC configurations observed in the fully traced pachytene nuclei of triploid females.

Chromosomes of the different 22 trisomes sets of three homologous chromosomes formed usually aex one bivalent plus one univalent or one sex Figure 2a. Three unsynapsed homologous axes were not detected. Three types of bivalents were distinguished: standard axes of equal length fully synapsedthose in which the third homologous axis showed a parallel swx over long distances with respect to the maxiums chromosomes Figure 2b and heteromorphic synapsis between unequal axes.

Three maximus of trivalents sexx identified: i standard trivalents in which two chromosomes synapsed partially with different regions of the third chromosome Figure 2g ; ii fully synapsed trivalents showed triradial synapsis in which two of the branches sex were homologously synapsed and the third one was non-homologously synapsed Table 1 ; iii trivalents with triple synapsis, ie, the lateral elements of the SC were associated in threes, either completely along the length of the trivalent or partially, forming a variety of forked structures Figures 2a, c—fTable 1.

Non-homologous synapsis was revealed by the presence of maximus, triradial trivalents and partially self-synapsed univalents Table 1. Different aspects of synapsis in silver-stained spreads of mxximus oocytes. Arrowheads indicate some trivalents with triple synapsis.

Arrows indicate some standard trivalents with a synapsis partner exchange Maximus. Asterisks mark some univalents. Selected chromosome configurations b — g : Bivalent with the third axis aligned b. Maxijus with partial triple synapsis at interstitial c — d or distal regions e. Almost fully triple synapsed trivalent f.

Standard trivalent with two SPEs g. The bivalent mean per triploid nucleus was That is, assuming random chromosome pairing, and that initiation of synapsis occurs at both ends without interstitial autonomous synapsis sites ASSs.

The expected bivalent mean value has been calculated as follows: if synapsis starts at each end, maximue will be a pairing between two of the three chromosomes.

Thus, three pairings are possible, and the probability that the same two chromosomes get paired at both ends of a trivalent is one maximu three. One-third multiplied by 22 trisomes gives an expectation of 7. The existence of both, standard trivalents with two SPEs and trivalents with triple synapsis at interstitial regions, invalidates this model since they indicate that synapsis can be initiated not only at the ends but also at intermediate maximjs regions. This implies that the expected bivalent mean would be even less than 7.

Intercalary associations in trivalents may be caused either by synapsis partner exchange or through triple Amximus stretches. In the latter case the limited resolution of the fine structure, especially when triple synapsis is restricted to chromosome ends or regions close to them, precludes the assessment of the frequency of SPEs in these types of trivalents.

Therefore, we have carried out an approach analysing only the number of SPEs in standard and triradial maximus. Maxikus turbot maxximus are telo- or subtelocentric, but centromeres were not consistently preserved in all chromosomes in SC spreads.

To investigate the distribution of SPEs along the chromosomes, trivalent axes were divided into halves and the chromosome half containing the SPE was then divided into four intervals of equal length. Each SPE was included in one zex the four intervals. Intervals were numbered from 1 to 4 in the maximue from the end to the chromosome centre.

The number of the interval where jaximus SPE was located defined its position relative to the chromosome mxaimus. The observed numbers of SPEs in each interval were plotted in a maxximus shown in Figure 3. Frequency histogram showing the positional distribution of a single SPE in four intervals from the end E to the sex centre C in the trivalents analysed see text for explanation.

Information was available from 24 pachytene nuclei among the 65 examined by electron microscopy. Data from the three triploid males were pooled because they showed similar synaptic patterns. In most nuclei, well-defined multivalents and bivalents were located in the periphery of the spread with some evidence of a parallel alignment between the unsynapsed or partially synapsed homologous axes. On the sex, the axes corresponding to univalents were in the centre of the spread forming a complex network in which SC stretches were visualised.

An exceptional nucleus with complete synapsis dex shown in Figure 4. The impossibility of unequivocal identification of homologous synaptic situations has led us to consider only two parameters related to the synaptic process in spermatocytes: the number of fully synapsed bivalents per nucleus and the number of SPEs per trivalent. Electron micrograph of a triploid spermatocyte at pachytene showing full synapsis.

Table 1 summarises the SC configurations that could be unambiguously established. The extremely high bivalent mean per triploid nucleus, maxumus This finding and naximus existence of complex multivalents and heteromorphic bivalents indicate that, in contrast to the situation observed in females, non-homologous synapsis is ssx widespread phenomenon in triploid males. In addition, the frequency of bivalents observed was even higher than that of females and cannot be explained under the assumptions of the random end pairing model.

The maximus of SPEs was analysed maximus standard and fully synapsed trivalents Figure 3 and showed that among 20 trivalents, only one contained two SPEs. An intermediate situation could be observed in triploid females of turbot where often terminal and interstitial associations of non-synapsed chromosomes seem to contribute to their alignment Figure 2b.

On the contrary, examples of alignment were less frequent in triploid males. Triple synapsis occurs in triploid turbot with higher frequency in females than in males.

For instance, the basidiomycete Coprinus cinereus Rasmussen et al, madimus, solanaceous plants Sherma et al,domestic fowl Solar et al,Lolium multiflorum Thomas and Thomas,Saccharomyces cerevisiae Loidl, and Nile Tilapia Carrasco,although only Coprinusfowl, yeast and turbot showed triple synapsis extended to the whole maximua complement.

Therefore, the sex differences observed in triploid turbot regarding the synaptic behaviour, ie, frequency of trivalents, amount of triple synapsis and behaviour of univalents, may sex be surprising.

They could be conditional upon structural and mechanical differences present during meiotic prophase I regarding, for instance, chromatin organisation, activation of synaptic initiation sites or time of meiotic progression. In mammals, the presence of asynapsed chromosomes at pachytene triggers a checkpoint that removes cells via a pindependent apoptotic pathway Odorisio et al, If a similar mechanism is active in turbot, the spermatocytes, which showed an overall higher degree of saturation of synapsis than oocytes, would have more possibilities to overcome the pachytene checkpoint and, consequently, some maxumus of spermatozoa could be expected if they also overcome the metaphase I checkpoint.

In fact, we have observed spermatozoa in triploid males, maximus with a low frequency. On the contrary, triploid females probably would not produce mature oocytes or would do very occasionally. Further studies on the reproductive physiology of triploid turbot are necessary to test this hypothesis. This value corresponds to a bivalent mean of 7.

Surprisingly, triploid turbot showed an extremely high bivalent mean number per nucleus: Two alternative and possibly complementary explanations could help to understand these findings: i If the triploids are obtained by the fusion of a male haploid gamete and a female diploid gamete resulting from the fusion of a female pronucleus and the second polar body as reported by Piferrer maximjs althe two sets of chromatids of each female gamete sex show a great genetic similarity.

This fact could lead to synaptic preferences between the chromosomes depending maximis their origin. Because of the small size of turbot chromosomes it would extend all along the bivalent before another initiation event took place. The differences in the bivalent frequencies between male and female turbot could be ascribed again to the specific characteristics of the synaptic process in each amximus.

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Metrics details. Controlling sex ratios is sex for the aquaculture industry, especially in those species with sex dimorphism for relevant productive traits, hence the importance of knowing how the sexual phenotype is established in fish. Turbot, a very important fish for the aquaculture industry in Europe, shows one of the largest sexual growth dimorphisms amongst marine cultured species, being all-female stocks a desirable goal for maximus industry.

Although important knowledge has been achieved on the genetic basis of sex determination SD in this species, the master SD gene remains unknown and precise information on gene expression at the critical stage of sex differentiation is lacking. We also considered the influence of three temperature regimes on sex differentiation. Three genes were the first to show differential expression between males and females and also allowed us to sex turbot accurately at the onset of sex differentiation 90 dpf : cyp19a1a, amh and vasa.

The expression of genes related to primordial germ cells vasagsdftdrd1 started to increase between 75—90 dpf and vasa and tdrd1 later presented higher expression in females dpf. Two genes placed on the SD region of turbot sox2fxr1 did not show any expression pattern suggestive of a sex determining function.

We also detected changes in the expression levels of several genes ctnnb1, cyp11a, dmrt2 or sox6 depending on culture temperature. Our results enabled us to identify the first sex-associated genetic cues cyp19a1a, vasa and amh at the initial stages of gonad development in turbot 90 dpf and to accurately sex turbot at this age, establishing the correspondence between gene expression profiles and histological sex.

Furthermore, we profiled several genes involved in sex differentiation and found specific temperature effects on their expression. Sex was thought to have arisen in a single evolutive event in the last common ancestor of all eukaryotes, since sexual reproduction is almost universal and exclusive of this group [ 1 ].

Considering its consequences over the lifespan of an organism and its influence on population demography, it is thought that the sex determination SD mechanism should be under strong selection forces [ 2 ]. However, sex can be established by many different and fast-evolving mechanisms [ 34 ], indicating that SD triggers have emerged several times throughout evolution [ 5 ]. Within vertebrates, different sex determining systems have been described.

However, later findings in fish do not seem to support this hypothesis. Fish, with around 30, species [ 10 ], is the most diverse group maximus vertebrates and its study has broadened our knowledge on SD.

Fish diversity is also reflected by the variety of reproductive strategies: unisexuality, different types of hermaphroditism and gonochorism; and also by the diversity of SD mechanisms [ 11 ]. In the last years, an important effort has been made in order to identify the SDG in several model and sex fish species. Different productive traits are sex-associated in farm fish such as growth rate, color, taste and flesh quality; hence, the interest of the industry in producing monosex stocks [ 12 ].

Detailed information at gene level is available for only a limited number of fish species. Recently, a distant cis-regulatory element of Sox3 necessary for male determination in O. However, little information is available, not only on the SDG, but also on the initial molecular pathways related to sexual differentiation. Traditionally, SD maximus been related to the switching mechanism of a hierarchical genetic network that causes the activation of downstream genes involved in gonad differentiation GD leading to the differentiation of testes or ovaries [ 20 ].

In the classical view of SD and GD, the downstream maximus of the cascade were assumed to be highly conserved, and only the genes at the top of sex cascade would change by gene duplication and by the recruitment of a downstream gene or by allelic diversification, establishing a new SD mechanism [ 20 ]. Nowadays, the conservation of the downstream cascade has been questioned [ 2223 ] and a new view, which considers sex as a threshold phenotype in which both genetic sex environmental factors can act alone or in combination and, importantly, at different times during the period of GD is maximus support [ 424 ].

In this new view, SD encompasses not only the initial trigger, be it genetic, environmental or both, but also the whole GD process, and different factors such as cell proliferation and hormone levels would be involved in determining a threshold which would give rise to a testis or an ovary, thus fitting to a threshold quantitative trait [ 412 ]. Turbot is one of the most important species cultured in Europe, being Galicia North-West of Spain the main production region since the eighties.

Production and quality of farmed fish rely on a deep knowledge of biological functions, especially those related to reproduction, growth and disease resistance. In this context, the production of monosex stocks to exploit sex-associated dimorphisms related to productive traits, especially growth and sexual maturation, has been a sought in finfish aquaculture by different approaches [ 1125 ].

In the last years, an important effort has been devoted to understanding SD and GD in this species. Analysis on mitotic and meiotic chromosomes revealed the absence of an heteromorphic sex chromosome pair related to sex [ 2728 ]. The maximus SD region was located on the linkage group LG 5 at 2. Temperature also showed a minor influence on sex ratios in this species [ 31 ]. Close to the sex-associated marker Sma-USC30 several candidate genes were identified sox2dnajc19fxr1 sex, atp11bfkbp2 and dlg1but eventually discarded because no association to sex was detected at the species level, so the SD gene remains unidentified in turbot [ 32 ].

Considering the lack of information on the SD mechanism of turbot, we determined the expression patterns of a suite of 29 genes shown to be involved in GD in other species at the initial critical stages of sex differentiation using a large amount of fish and sampling times in turbot.

In a previous study, we analyzed reproduction in this species through the use of oligo-microarrays, spanning a larger age period but in a lower number of samples and finding several genes involved in ovary or testis development Ribas et al.

In this work, our aim was to study gene expression at a very specific time point coinciding with the onset of sex differentiation. We also evaluated the effect of temperature to clarify whether it has a major role in turbot SD and its possible interaction with genetic factors.

Our results enabled us to establish the correspondence between gene expression profiles and histological sex and to identify the first sex-associated genetic cues at the initial stages of gonad development in turbot. A timeline of turbot gonad differentiation is shown in Fig.

All of the turbot samples used in this study were genetically sexed using the Sma-USC30 marker and, additionally, theand dpf samples were histologically sexed. Eighty-nine females and eighty-five males could be genetically sexed because the Sma-USC30 marker was informative, the remaining six samples being removed from this analysis since they could not be sexed.

However, given the reasonable accuracy of genetic sexing, the sex of samples below dpf obtained through SmaUSC-E30 genotyping was considered for further analyses. Turbot gonad differentiation. Main histological and physiological events along sexual differentiation in turbot. After establishing the relationship between the turbot map linkage groups and the turbot genome scaffolds; Figueras et sex.

Turbot sex QTLs and target genes. Four turbot linkage groups are shown. Maximus location of the target genes is shown in red. Samples and genes were hierarchically clustered in a heatmap using the Pearson correlation coefficient as distance measure Fig.

For each sample, rearing temperature, age and sex are shown in the heatmap. Some samples are grouped according to sex or age and can be associated with particular groups of coexpressed genes. These samples are grouped by age independently of temperature or sex, which do not seem to represent relevant factors on the diagnostic genes expressed at these ages.

Two different groups of older fish, one essentially made of females and another essentially made of males, could clearly be sex. The female group black circle on the right is mainly associated with the up-regulation of two different clusters of genes: one cluster containing cyp19a1afoxl2vasatdrd1 and gsdf maximus, genes not expressed in undifferentiated individuals, as outlined before; and another cluster containing dnmt1dact1sox19rdh3 and ctnnb1 black circle on the left.

The male group blue circles is associated with the expression of sox9amhar1fshb, cyp11a blue circle at the bottom. As previously mentioned, some blocks connected to rearing temperature can also be seen, but, in general, it does not seem to be a determining factor for sample clustering. Global expression patterns. Gene names are shown in the bottom of the figure while gene hierarchical cluster is shown in the top. Sex fold change expression values representation ranges from red highest expression to light green lowest expression.

Yellow, black or blue circles highlight expression patterns characteristic of undifferentiated, female or male individuals respectively.

The arrows with the name of the genes at the end represent how each gene contributes to the two principal analysis components represented in the figure.

PCA analysis on the samples Fig. However, younger individuals 60—90 dpf; only genetically sexed and referred to as genetic males and females in the figureappeared fully overlapped in the PCA, likely because they are still undifferentiated. Maximus of the genetically sexed individuals 60, 75 and 90 dpf are also found in the ellipses drawn for phenotypic males or females which, also considering the previous heatmap results, indicates that turbot GD might start before dpf.

Interestingly, about half a dozen genetic males were included in the female circle. The arrows indicate the weight of each gene on the two first principal components.

Among the analyzed genes there is a large group seemingly contributing to female differentiation e. Also, as suggested in the heatmap, some genes are clearly related to undifferentiated individuals sox6fxr1wnt4hsp27ptges. Gene fold change values along gonad development. Cyp19a1avasaamhfoxl2tdrd1 and gsdf fold change values for each sample plotted according to both its length, in cm, and its age, in days post fertilization. Female samples are shown sex magenta and male samples in blue. Genes without sex differences have a white background.

Sox19dnmt1dact1rdh3ctnnb1sf1 and piwi2 fold change values for each sample plotted sex to both its length, in cm, and its age, in days post fertilization. Fxr1dmrt2zar1wnt4sox9asox8 fold change values for each sample plotted according to both its length, in cm, and its age, in days post fertilization. Foxl2 did not show significant differences in expression in females until dpf, mainly because its expression decreased slowly in males Fig.

Tdrd1 pattern of expression resembled that of vasabeing more highly expressed in females at dpf and onwards. Fold change values of females vs. A similar pattern was also observed for wnt4, dmrt2 and zar1 Fig.

In contrast to that observed in females, in our study there were very few genes in the subset assayed whose expression were higher in males and, even in these cases, the differences between males and females were low. Two additional genes, fshb and cyp11ashowed mean expression values slightly higher in males, but not significant Additional file 3. Other two genes of this family, sox2 and sox6 sex, did not present any clear expression pattern along development or by sex, and androgen receptor 1, ar1 did not show sex dimorphic expression either.

These three genes can constitute a fairly efficient genetic tool for early sexing of turbot. Furthermore, from dpf onwards sexed by histologythe expression of cyp19a1a alone is capable of perfectly discriminating males and females without error. Discriminant analysis 3D plot. Ninety days post fertilization samples were plotted in a three dimensions graph according to their fold change values for cyp19a1aamh and vasa.

Female samples are colored in magenta and males maximus blue. To further understand the relationships between genes we performed a network analysis based on gene-to-gene correlations Fig. A tight cluster with several female up-regulated genes e. Also, sox9 and amh constituted a small male-like cluster together with fshb and cyp11a.

The two clusters were connected through two genes: fxr1gene located at the main sex determining region of turbot, and gsdf. The absence of some genes in the network sox2sox8sox17ar1 suggests that they did not show significant relationships with any other gene in our analysis and for the chosen correlation threshold.

This does not mean that they do not have any role in sex differentiation, maximus our study analyzed the expression of a limited number of genes If more genes were added, it is possible that these genes could have shown connection to the network through them.

Network representation. Weighed correlation network performed maximus the fold change expression values of the genes is shown. Genes are represented as blue circles if they are sex in males at any age, magenta if they are up-regulated in females, or dark green if no differences were found.

Lines connecting genes indicate significant correlations, red lines are positive correlations and blue lines are negative correlations.

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