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Histology of ovary and testis of Nile tilapia exposed to control (28°C) and high temperature (36°C). Histology of the control (28°C) (A) and high temperature (36°C) treated; (B) fish ovary after extended rearing of high temperature treated fish in the water at normal temperature for 188 days, with decrease of germ cells in high temperature treated fish ovary H&E×100; (C, D) Histology of the control (28°C); (C) and high temperature (36°C) treated; (D) fish testis after extended rearing of high temperature treated fish in the water at normal temperature for 188 days H&E×400.Scalebars represent 10 μm. PVO = oocytes at the pre-vitellogenic stage; VO = oocytes at the vitellogenic stage; SP = spermatocyte; SZ = spermatozoa; SC = Sertoli cells; *: abnormally developed oocyte.
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In some fish species, high or low temperature can switch the sex determination mechanisms and induce fish sex reversal when the gonads are undifferentiated. During this high or low temperature-induced sex reversal, the expressions of many genes are altered. However, genome-wide DNA methylation changes in fish gonads after high or low temperature tr...
Citations
... Previous studies have found that a short-term high temperature treatment can induce sex reversal in most XX tilapia during the critical period of sex differentiation [8,11]. Sun et al. [12] showed that a high-temperature treatment of sexually undifferentiated Nile tilapia significantly affected DNA methylation and the transcript levels of many genes related to sex differentiation in the gonad tissue. However, it has been suggested that there is sexual dimorphism in the expression of genes in the brain that might have an essential role in responding to gonadal differentiation [13]. ...
... Plusieurs travaux se sont intéressés à l'analyse de l'effet des traitements thermiques sur la différenciation gonadique au niveau histologique (cellules germinales), génétique (gènes majeurs) et physiologique (stéroïdes hormonales) (D'Cotta et al., 2001;Bezault et al., 2007;Baroiller et al., 2009a, Nivelle et al., 2019Alba et al., 2023). D'autres se sont intéressés à l'analyse de l'influence de la température sur l'évolution des cellules germinales à différentes étapes de la spermatogénèse chez les néomâles XX et les mâles normaux XY du tilapia du Nil (Vilela et al., 2003;De Alvarenga et De França, 2009;Melo et al., 2016;Sun et al., 2016Sun et al., , 2018Jin et al., 2019;Wang et al., 2019;Dussenne et al., 2020;Zhao et al., 2020). Quelques travaux ont également montré une féminisation des mâles YY du tilapia du Nil par des hautes températures (36°C) (Abucay et al., 1999;Karayücel et al., 2003), indiquant un effet de la température dépendant du génotype sexuel. ...
Le tilapia du Nil est une espèce aquacole majeure dont la gamétogénèse est fortement modulée par la température. Ainsi, de nombreux travaux ont été consacrés à l’étude de l’influence des traitements thermiques sur la spermatogénèse chez cette espèce. Le présent article a pour objectif de faire un état des connaissances de l’influence de la température sur la spermatogénèse chez le tilapia du Nil. Les connaissances disponibles sur l’organisation testiculaire, l’évolution des cellules germinales et le rôle des cellules somatiques chez le tilapia de Nil ont d’abord été présentées. Les travaux relatifs aux effets de la température sur la spermatogénèse chez cette espèce ont ensuite été synthétisés à quatre niveaux à savoir l’influence des basses températures (≤ 20°C), les hautes températures (35°C) chez les mâles matures, les hautes températures de masculinisation (36°C) et les hautes températures stérilisantes (37°C). Les différents travaux concordent avec le fait que les basses températures compromettent l’évolution de la spermatogénèse chez le tilapia du Nil tandis que les hautes températures accélèrent la spermatogénèse chez les mâles matures. Il ressort également que l’influence des traitements thermiques d’inversions sexuelles ou de stérilisations sur les cellules germinales, serait corrélée avec la variabilité inter ou intra souche de la thermosensibilité de la différenciation sexuelle. English title: Influence of temperature on Nile tilapia spermatogenesis, Oreochromis niloticus (Linnaeus, 1758): a synthesis Temperature highly modulates gametogenesis of a Nile tilapia which is the major aquaculture species. Many studies have therefore been devoted to studying the influence of thermal treatments on spermatogenesis in this species. This article reviews what is known about the influence of temperature on spermatogenesis in Nile tilapia. Available knowledge on the testicular organization, germ cells evolution and the role of somatic cells in Nile tilapia was first presented. Studies on the effect of temperature on spermatogenesis in this species was then synthesized at four levels, namely the influence of low temperatures (≤ 20°C), high temperatures (35°C) in mature males, masculinization high temperatures (36°C) and high sterilizing temperatures (37°C). The various studies were consistent with the fact that low temperatures compromise the evolution of spermatogenesis in Nile tilapia, while high temperatures accelerate spermatogenesis in mature males. It is also evident that influence of heat treatments for sexual inversion or sterilization would be correlated with inter or intra-strain variability of thermosensivity in sexual differentiation.
... Thus, searching for informative epimarkers is at the frontier of aquaculture-related research. The effects of temperature in altering DNA methylation levels in some canonical sex-related genes associated with the masculinization of the population have been shown in many farming fish species: in the European sea bass [47][48][49], Nile tilapia (Oreochromis niloticus) [50,51], turbot (Scophthalmus maximus) [52], half-smooth tongue sole (Cynoglossus semilaevis) [53], and the Japanese flounder (Paralichthys olivaceus) [54]. ...
Rearing density directly impacts fish welfare, which, in turn, affects productivity in aquaculture. Previous studies have indicated that high-density rearing during sexual development in fish can induce stress, resulting in a tendency towards male-biased sex ratios in the populations. In recent years, research has defined the relevance of the interactions between the environment and epigenetics playing a key role in the final phenotype. However, the underlying epigenetic mechanisms of individuals exposed to confinement remain elucidated. By using zebrafish (Danio rerio), the DNA methylation promotor region and the gene expression patterns of six genes, namely dnmt1, cyp19a1a, dmrt1, cyp11c1, hsd17b1, and hsd11b2, involved in the DNA maintenance methylation, reproduction, and stress were assessed. Zebrafish larvae were subjected to two high-density conditions (9 and 66 fish/L) during two periods of overlapping sex differentiation of this species (7 to 18 and 18 to 45 days post-fertilization, dpf). Results showed a significant masculinization in the populations of fish subjected to high densities from 18 to 45 dpf. In adulthood, the dnmt1 gene was differentially hypomethylated in ovaries and its expression was significantly downregulated in the testes of fish exposed to high-density. Further, the cyp19a1a gene showed downregulation of gene expression in the ovaries of fish subjected to elevated density, as previously observed in other studies. We proposed dnmt1 as a potential testicular epimarker and the expression of ovarian cyp19a1a as a potential biomarker for predicting stress originated from high densities during the early stages of development. These findings highlight the importance of rearing densities by long-lasting effects in adulthood conveying cautions for stocking protocols in fish hatcheries.
... The role of DNA methylation in regulating gene expression has been described under diverse contexts including toxicology (i.e. Kamstra et al., 2015) and sex change (Navarro-Martín et al., 2011;Parrott et al., 2014;Sun et al., 2016). The gene expression of a particular gene can increase or decrease based on the location of the DNA methylation. ...
Understanding the molecular mechanisms underlying individual responses to environmental changes is crucial for species conservation and management. Pelagic fishes including Atlantic herring ( Clupea harengus ) are of particular interest because of their key ecological and economic roles and their susceptibility to a changing ocean from global warming. Temperature and photoperiod have been linked with spawning time and location in adult herring, but no study has thus far investigated the role of environmental factors on gene regulation during the vulnerable early developmental stages. Here, we examine DNA methylation patterns of larval herring bred under two temperatures (11°C and 13°C) and photoperiod (6 and 12 h) regimes in a 2 × 2 factorial design. We found consistently high levels of global methylation across all individuals and a decline in global methylation with increased developmental stage that was more pronounced at 13°C ( p ≤ 0.007) than at 11°C ( p ≥ 0.21). Most of the differentially methylated sites were in exon and promoter regions for genes linked to metabolism and development, some of which were hypermethylated at higher temperature. These results demonstrate the important role of DNA methylation during larval development and suggest that this molecular mechanism might be key in regulating early‐stage responses to environmental stressors in Atlantic herring.
... The mechanisms that sex determination and differentiation in teleosts are broadly classified as environmental sex determination (ESD), genetic sex determination (GSD), and combining ESD and GSD. 2 Another potential way to regulate sex determination is DNA methylation. 3,4 DNA methylation occurs in the genomes of a wide array of bacteria, plants, fungi, and animals. DNA methylation in vertebrates typically occurs at cytosine-phosphate-guanine sites (CpG) and is catalyzed by DNA methyltransferase. ...
... Global DNA methylation level increases in Nile tilapia gonads during high temperature-induced masculinization. 4 DNA methylation of the cytochrome P450 family 19 subfamily A polypeptide 1a (cyp19a1a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. 31 The DNA methylation inhibitor 5-aza-2-deoxycytidine reversed the natural sex change of Monopterus albus. ...
We identified that the genes heat shock transcription factor 5 (hsf5) and ring finger protein 43 (rnf43) happened fusion in Nile tilapia (Oreochromis niloticus), called hsf5-rnf43, and provided the characteristic and functional analysis of hsf5-rnf43 gene in fish for the first time. Analysis of spatiotemporal expression showed that hsf5-rnf43 was specifically expressed in the testis and located in primary spermatocytes of adult Nile tilapia and gradually increased during testis development from 5 to 180 days after hatching. We also found DNA methylation regulated sex-biased expression of hsf5-rnf43 in the early development of Nile tilapia, and was affected by high temperature during the thermosensitive period of Nile tilapia sex differentiation. Therefore, we first reported that the fusion gene hsf5-rnf43 was sex-biased expressed in the testis regulated by DNA methylation and affected by high temperature, which may be involved in the maintenance of testis function and sex differentiation of Nile tilapia.
... Thermal and hypoxia stress induce rapid changes in global DNA methylation. In this study and others [14][15][16][17][33][34][35][36][37][38] , DNA methylation demonstrates responsiveness to warm temperature acclimation, but whether rapid changes in methylation occur in response to acute high temperature and hypoxia exposures, and whether heatwave exposure affects these responses is unknown in fishes. For gill DNA methylation, two-way ANOVA detected significant effects of CTMax ( Fig. 8a; P < 0.0005), no significant effect of acclimation condition (pre-heatwave vs heatwave; P > 0.05), and a significant interaction between the two factors (P < 0.005). ...
Heatwaves are increasing in frequency and severity, posing a significant threat to organisms globally. In aquatic environments heatwaves are often associated with low environmental oxygen, which is a deadly combination for fish. However, surprisingly little is known about the capacity of fishes to withstand these interacting stressors. This issue is particularly critical for species of extreme conservation concern such as sturgeon. We assessed the tolerance of juvenile white sturgeon from an endangered population to heatwave exposure and investigated how this exposure affects tolerance to additional acute stressors. We measured whole-animal thermal and hypoxic performance and underlying epigenetic and transcriptional mechanisms. Sturgeon exposed to a simulated heatwave had increased thermal tolerance and exhibited complete compensation for the effects of acute hypoxia. These changes were associated with an increase in mRNA levels involved in thermal and hypoxic stress (hsp90a, hsp90b, hsp70 and hif1a) following these stressors. Global DNA methylation was sensitive to heatwave exposure and rapidly responded to acute thermal and hypoxia stress over the course of an hour. These data demonstrate that juvenile white sturgeon exhibit substantial resilience to heatwaves, associated with improved cross-tolerance to additional acute stressors and involving rapid responses in both epigenetic and transcriptional mechanisms.
... Mounting evidence in teleosts also shows that culture conditions or environment affect embryogenesis and early development including sex determination and differentiation, gamete quality, sex ratio, egg size, larvae survival, growth, etc., through epigenetic mechanisms [94]. Temperature can impact the sex determination and differentiation of many heat-sensitive teleost species by affecting the methylation level of typical sex-specific molecules and interfering with the interaction between transcriptional elements [236][237][238][239][240][241]. Studies also show that temperature affects the sex ratio of some fish species in natural environments via epigenetic mechanisms (Chapter 5). ...
As aquaculture and livestock production and human demands increase, much effort has been focused on improving production efficiency, health and well-being of agricultural animals and fish, as well as their sustainability using genetic approaches, which have explained part of the phenotypic variability of economic traits. Mounting evidence from epigenetic research in humans and animals has demonstrated that epigenetics plays a complementary role to genetics, touching many aspects of biological processes such as reproduction, early development, disease, growth, and nutrition. The role of epigenetics in aquaculture and aquatic animals is similar to other vertebrates in principle, even for embryonic development. As epigenetics in aquaculture is behind other livestock and animals, in this chapter, we will briefly review the potential roles and applications of epigenetic processes in reproduction and early development, health and well-being management, and nutrition and growth advancement, and sustainability enhancement from different taxa to diverse teleosts, aimed to provide insights into the potential role of epigenetics in aquaculture and aquatic animals, based on most recently research progress.
... Whilst such studies identified CREs at particular loci, epigenetic sequencing methods can capture chromatin accessibility and transcription factor (TF) binding at the genome-wide level [14]. Only a handful of studies, all using DNA methylation, have applied epigenetic approaches to study adaptive traits in tilapia [15]; this includes the regulation of tilapia growth [16][17][18], sexual dimorphism [19], and sex determination [20,21]. ChiP-seq approaches have also been used to map active promoter elements associated with Nile tilapia fin development [22]. ...
The Nile tilapia (Oreochromis niloticus) accounts for ~9% of global freshwater finfish production however, extreme cold weather and decreasing freshwater resources has created the need to develop resilient strains. By determining the genetic bases of aquaculture relevant traits, we can genotype and breed desirable traits into farmed strains. We generated ATAC-seq and gene expression data from O. niloticus gill tissues, and through the integration of SNPs from 27 tilapia species, identified 1168 highly expressed genes (4% of all Nile tilapia genes) with highly accessible promoter regions with functional variation at transcription factor binding sites (TFBSs). Regulatory variation at these TFBSs is likely driving gene expression differences associated with tilapia gill adaptations, and differentially segregate in freshwater and euryhaline tilapia species. The generation of novel integrative data revealed candidate genes e.g., prolactin receptor 1 and claudin-h, genetic relationships, and loci associated with aquaculture relevant traits like salinity and osmotic stress acclimation.
... As methylated cytosines undergo spontaneous deamination resulting in C to T (thymine) mutations, the abundance of CpG dinucleotides is reduced over evolutionary time from the expectation based on the frequency of Cs and Gs in the genome [6,7]. Various studies demonstrated that DNA methylation is sexually dimorphic in the developing or posthatching gonads of vertebrates with temperature-dependent sex determination (TSD), including turtles [6,[8][9][10][11] and alligator [12], and in fish with a mixed system of genotypicsex determination susceptible to thermal effects (GSD + TE) [13][14][15]. These observations raise the possibility that DNA methylation, if it were sexually dimorphic in somatic tissues, could be used as a non-lethal sex diagnostic. ...
Background: The gonads of Chrysemys picta, a turtle with temperature-dependent sex determination (TSD), exhibit differential DNA methylation between males and females, but whether the same is true in somatic tissues remains unknown. Such differential DNA methylation in the soma would provide a non-lethal sex diagnostic for TSD turtle hatchings who lack visually detectable sexual dimorphism when young. Methods: Here, we tested multiple approaches to study DNA methylation in tail clips of Chrysemys picta hatchlings, to identify differentially methylated candidate regions/sites that could serve as molecular sex markers To detect global differential methylation in the tails we used methylation-sensitive ELISA, and to test for differential local methylation we developed a novel hybrid method by sequencing immunoprecipitated and bisulfite converted DNA (MeDIP-BS-seq) followed by PCR validation of candidate regions/sites after digestion with a methylation-sensitive restriction enzyme. Results: We detected no global differences in methylation between males and females via ELISA. While we detected inter-individual variation in DNA methylation in the tails, this variation was not sexually dimorphic, in contrast with hatchling gonads. Conclusions: Results highlight that differential DNA methylation is tissue-specific and plays a key role in gonadal formation (primary sexual development) and maintenance post-hatching, but not in the somatic tail tissue.
... However, with channel catfish, only pseudo-females (sex reversal of genetic males to phenotypic females) have been achieved, no matter what the treatments were. With many fish species, such as zebrafish (25), medaka (26), tilapia (27), and half-smooth tongue sole (28), androgen and high-temperature treatment led to sex reversal into pseudo-males, but these treatments led to sex reversal of males into pseudo-females with channel catfish (19,23), suggesting that channel catfish may have a unique mechanism for sex determination. ...
The X and Y chromosomes of channel catfish have the same gene contents. Here, we report allelic hypermethylation of the X chromosome within the sex determination region (SDR). Accordingly, the X-borne hydin-1 gene was silenced, whereas the Y-borne hydin-1 gene was expressed, making monoallelic expression of hydin-1 responsible for sex determination, much like genomic imprinting. Treatment with a methylation inhibitor, 5-aza-dC, erased the epigenetic marks within the SDR and caused sex reversal of genetic females into phenotypic males. After the treatment, hydin-1 and six other genes related to cell cycle control and proliferative growth were up-regulated, while three genes related to female sex differentiation were down-regulated in genetic females, providing additional support for epigenetic sex determination in catfish. This mechanism of sex determination provides insights into the plasticity of genetic sex determination in lower vertebrates and its connection with temperature sex determination where DNA methylation is broadly involved.
