Differential expression analysis of genes involved in high-temperature induced sex differentiation in Nile tilapia

Li, Chun Ge; Wang, Hui; Chen, Hong Ju; Zhao, Yan; Fu, Pei; Ji, Xiang

doi:10.1016/j.cbpb.2014.08.006

Cited by 35 publications

(22 citation statements)

References 57 publications

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“…47 Nile tilapia, Oreochromis niloticus, exposed to high temperatures show only a negative correlation between cyp19a1a expression and expression of four hsps, including hsp70, in ovaries. 48 In our study, increased expression of hsp70, which was upregulated initially during the maximum temperatures in our Δ8°C 12-h treatment, could have enhanced cyp19a expression, in turn increasing estrogen synthesis. However, it is unclear whether these mechanisms led to sex reversal in our study because only a small percentage of fish underwent sex reversal where reversal was nondirectional.…”

Section: ■ Discussionmentioning

confidence: 81%

Fluctuating Water Temperatures Affect Development, Physiological Responses and Cause Sex Reversal in Fathead Minnows

Coulter

Höök

Mahapatra

et al. 2015

Environ. Sci. Technol.

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Natural and human activities can result in both high temporal and spatial variability in water temperature. Rapid temperature changes have the potential to dramatically affect physiological processes in aquatic organisms and, due to their limited mobility, fish early life stages are particularly vulnerable to ambient temperature fluctuations. In this study, we examined how the magnitude and frequency of temperature fluctuations affect survival, growth, development, expression of thermoresponsive genes, and gonadal differentiation in fathead minnows, Pimephales promelas. We exposed individuals (0 to 4 days post fertilization) of known genotypic sex to fluctuations of Δ4 °C over 12-h, Δ8 °C over 12- and 24-h, and three stable temperatures (21, 25, and 29 °C) for up to 45 d. Expression of hsp70 in fish exposed to the highest-magnitude, highest-frequency fluctuating treatment cycled in concert with temperature and was upregulated initially during exposure, and may have contributed to temperature fluctuations having little effect on time to and size at hatching (whole-organism responses). This treatment also caused fish to undergo nondirectional sex reversal. These results indicate that hsp70 may be involved in mediating thermal stress from subdaily temperature fluctuations and that sex determination in fathead minnows can be influenced by cycling temperatures.

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Section: ■ Discussionmentioning

confidence: 81%

Fluctuating Water Temperatures Affect Development, Physiological Responses and Cause Sex Reversal in Fathead Minnows

Coulter

Höök

Mahapatra

et al. 2015

Environ. Sci. Technol.

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“…In 2011, Navarro-Martín et al first described DNA methylation of cyp19a (cytochrome P450, family 19, subfamily a), which regulated the cyp19a mRNA expression, and temperature effects on sex ratios in European sea bass [ 5 ]. During high or low temperature-induced sex reversal in fish species, the expressions of many genes are altered, such as cyp19a1a , foxl2 (forkhead box L2), sox9 (sex-determining region Y box 9), dmrt1 (doublesex and mab-3 related transcription factor 1), ERα , and ERβ [ 6 – 11 ]. Thus, a high or low temperature could cause a global change of DNA methylation and gene expression.…”

Section: Introductionmentioning

confidence: 99%

Global DNA Methylation Changes in Nile Tilapia Gonads during High Temperature-Induced Masculinization

et al. 2016

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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 treatment are unclear. Herein, we compared the global DNA methylation changes in the gonads from control females (CF), control males (CM), high temperature-treated females (TF), and high temperature-induced males (IM) from the F8 family of Nile tilapia (Oreochromis niloticus) using methylated DNA immunoprecipitation sequencing. The DNA methylation level in CF was higher than that in CM for various chromosomes. Both females and males showed an increase in methylation levels on various chromosomes after high-temperature induction. We identified 64,438 (CF/CM), 63,437 (TF/IM), 98,675 (TF/CF), 235,270 (IM/CM) and 119,958 (IM/CF) differentially methylated regions (DMRs) in Nile tilapia gonads, representing approximately 0.70% (CF/CM), 0.69% (TF/IM), 1.07% (TF/CF), 2.56% (IM/CM), and 1.30% (IM/CF)of the length of the genome. A total of 89 and 65 genes that exhibited DMRs in their gene bodies and promoters were mapped to the Nile tilapia genome. Furthermore, more than half of the genes with DMRs in the gene body in CF/CM were also included in the IM/CM, TF/CF, TF/IM, and IM/CF groups. Additionally, many important pathways, including neuroactive ligand-receptor interaction, extracellular matrix-receptor interaction, and biosynthesis of unsaturated fatty acids were identified. This study provided an important foundation to investigate the molecular mechanism of high temperature-induced sex reversal in fish species.

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“…Regardless of the actual underlying sex-determining mechanism, a shared characteristic of all fish species in which temperature can alter sex ratios is that exposure to heat during early development upregulates the expression of genes related to testis differentiation with a concomitant down-regulation of genes related to ovarian differentiation, as assessed in several species (e.g., 9,13,[15][16][17]. This results in an increase in the proportion of males (18) and implies that some genetic females (XX or ZW females) in CSD species, or fish that otherwise would develop as females in a PSD system, end up developing as phenotypic males despite their genetic makeup.…”

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confidence: 99%

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

Ribas

Liew

Díaz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

119

136

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Understanding environmental influences on sex ratios is important for the study of the evolution of sex-determining mechanisms and for evaluating the effects of global warming and chemical pollution. Fishes exhibit sexual plasticity, but the underlying mechanisms of environmental effects on their reproduction are unclear even in the well-established teleost research model, the zebrafish. Here we established the conditions to study the effects of elevated temperature on zebrafish sex. We showed that sex ratio response to elevated temperature is family-specific and typically leads to masculinization (female-to-male sex reversal), resulting in neomales. These results uncovered genotype-by-environment interactions that support a polygenic sex determination system in domesticated (laboratory) zebrafish. We found that some heat-treated fish had gene expression profiles similar to untreated controls of the same sex, indicating that they were resistant to thermal effects. Further, most neomales had gonadal transcriptomes similar to that of regular males. Strikingly, we discovered heat-treated females that displayed a normal ovarian phenotype but with a "male-like" gonadal transcriptome. Such major transcriptomic reprogramming with preserved organ structure has never been reported. Juveniles were also found to have a male-like transcriptome shortly after exposure to heat. These findings were validated by analyzing the expression of genes and signaling pathways associated with sex differentiation. Our results revealed a lasting thermal effect on zebrafish gonads, suggesting new avenues for detection of functional consequences of elevated temperature in natural fish populations in a global warming scenario.A major paradox in developmental biology is the lack of conservation of sex-determining mechanisms even in closely related taxa (1). Thus, in mammals and birds, sex is genetically canalized by a chromosomal sex determination (CSD) system of male (XX/XY in mammals) or female (ZW/ZZ in birds) heterogamety, driven by the action of a master sex-determining gene: sry in mammals and dmrt1 in birds (1). In contrast, fish sex can be very plastic, with the combination of genetic and environmental influences (2). In addition to fish species with CSD, there are species with polygenic sex determination (PSD), in which sex depends on the combined action of several promale and profemale genetic factors, and species with temperature-dependent sex determination (TSD) (3). Understanding how the environment influences sex ratios in vertebrates is of fundamental importance in the study of the evolution of sex-determining mechanisms (4, 5). It is also of practical relevance in evaluating the effects of climate change and chemical pollution (6, 7).The effects of temperature on gene expression during sex differentiation have been investigated in different teleost species, including the African catfish, Clarias gariepinus (8), European sea bass, Dicentrarchus labrax (9, 10), Japanese flounder, Paralichthys olivaceus (11), pejerrey, Odontesthes...

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Differential expression analysis of genes involved in high-temperature induced sex differentiation in Nile tilapia

Cited by 35 publications

References 57 publications

Fluctuating Water Temperatures Affect Development, Physiological Responses and Cause Sex Reversal in Fathead Minnows

Fluctuating Water Temperatures Affect Development, Physiological Responses and Cause Sex Reversal in Fathead Minnows

Global DNA Methylation Changes in Nile Tilapia Gonads during High Temperature-Induced Masculinization

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

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