Expression profile and estrogenic regulation of anti‐Müllerian hormone during gonadal development in pejerrey <i>Odontesthes bonariensis</i>, a teleost fish with strong temperature‐dependent sex determination

Fernandino, Juan Ignacio; Hattori, Ricardo Shohei; Kimura, Hiroyuki; Strüssmann, Carlos Augusto; Somoza, Gustavo M.

doi:10.1002/dvdy.21731

Cited by 89 publications

(83 citation statements)

References 29 publications

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“…This difference represents just a fraction (8%) of the ∼15,000 DETs that were differentially expressed between untreated females (FCT) and males (MCT), which, in turn, account for a significant part of the estimated number of protein-coding genes (>25,000) in zebrafish. In fish, masculinization by elevated temperature usually involves down-regulation of profemale genes, such as cyp19a1a and foxl2, and up-regulation of promale genes, such as dmrt1 or amh (8)(9)(10)(11)(12)(13)(14). In accordance with this general pattern, the FHT2 females with a male-like gonadal transcriptome exhibited down-regulation of both key profemale genes such as cyp19a1a and vtg5 as well as downregulation of profemale pathways such as oocyte meiosis, progesterone-mediated oocyte maturation, canonical Wnt signaling (28,53), and Fanconi anemia (26).…”

Section: Discussionmentioning

confidence: 99%

“…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 bonariensis (12), and Nile tilapia, Oreochromis niloticus (13,14). 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].…”

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confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

mentioning

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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“…In pejerrey, the critical or temperature-sensitive period occurs from the first to the fifth week after hatching, depending on temperature. Pejerrey larvae reared from hatching at 13-19ºC produced 100% females, at 29ºC 100% males, and mixed sex proportions at intermediate temperatures, 24-25ºC (Strüssmann et al, 1996b(Strüssmann et al, , 1997Karube et al, 2007;Fernandino et al, 2008a). Sex differentiation is also accelerated by rearing temperature; the ovarian differentiation occurs before at 24ºC than at 17ºC, whereas testis development takes place before at 29ºC than at 24ºC (Ito et al, 2005;Fernandino et al, 2008b).…”

Section: Introductionmentioning

confidence: 97%

The effect of rearing temperature in larval development of pejerrey, Odontesthes bonariensis: morphological indicators of development

et al. 2011

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It is well known that in pejerrey water temperature not only affects growth rates but also directs the sexual differentiation process. This fact rise the question of how different the development of pejerrey larvae of the same age is when reared at different temperatures. A description of developmental stages for the embryonic and larval periods of the pejerrey, Odontesthes bonariensis, and the influence of rearing temperature on larval development are presented. Then, larval development was studied at three rearing temperatures, and changes in general morphology, fin morphology, and caudal fin structure have been taken into consideration within the thermal range involved in the temperature sex determination of this species. Fin fold reabsorption, caudal fin formation, and body shape were selected to follow the events leading to the acquisition of the juvenile morphology. The juvenile phenotype was defined when the fin fold was reabsorpted and the caudal fin acquired its definitive homocercal structure. The moment at which the juvenile phenotype was achieved, was evaluated in relation to larval age, size and, shape. The size resulted as the best indicator of development in pejerrey.A temperatura da água não afeta apenas as taxas de crescimento no peixe-rei, mas também direciona o processo de diferenciação sexual. Este fato levanta o questionamento de quão diferente é o desenvolvimento de larvas do peixe-rei da mesma idade quando criadas em temperaturas diferentes. Este trabalho teve como objetivo apresentar uma descrição do de desenvolvimento de embriões e larvas do peixe-rei, Odontesthes bonariensis, e a influência da temperatura de criação no desenvolvimento das larvas. Neste trabalho, o desenvolvimento das larvas foi estudado em três temperaturas diferentes de cultivo. Foram consideradas as alterações ocorridas na morfologia geral, assim como na morfologia e na estrutura da nadadeira caudal dentro da variação termal da temperatura de determinação sexual desta espécie. A taxa de reabsorção da membrana embrionária, a formação da cauda e o formato do corpo foram selecionados para acompanhar os eventos que levam à aquisição da morfologia juvenil. O fenótipo juvenil foi definido quando a nadadeira caudal foi reabsorvida e a cauda adquiriu a estrutura homocerca. O momento no qual o fenótipo juvenil foi atingido, foi avaliado quanto à idade, tamanho e formato da larva, sendo que o tamanho resultou no melhor indicador do desenvolvimento do peixe-rei.

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“…In some higher eukaryotes, environmental changes can drive major changes in phenotype. For example sex determination in some fish is temperature sensitive (Fernandino et al 2008;Marshall Graves 2008;Ospina-Alvarez & Piferrer 2008), while appropriately timed flowering in some plants requires exposure to a cold period, a process known as vernalization (Finnegan et al 2004;Shindo et al 2006). Nonetheless, for most cells in higher eukaryotes, the environment in which they exist is determined by the physiology and metabolism of the organism and of the cells in their immediate neighbourhood.…”

Section: Introductionmentioning

confidence: 99%

Epigenetic responses to environmental change and their evolutionary implications

Turner

2009

Phil. Trans. R. Soc. B

228

171

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Chromatin is a complex of DNA, RNA, histones and non-histone proteins and provides the platform on which the transcriptional machinery operates in eukaryotes. The structure and configuration of chromatin are manipulated by families of enzymes, some catalysing the dynamic addition and removal of chemical ligands to selected protein amino acids and some directly altering or displacing the basic structural units. The activities of many of these enzymes are sensitive to environmental and metabolic agents and can thereby serve as sensors through which environmental agents can alter gene expression. Such changes can, in turn, precipitate either local or cell-wide changes as the initial effect spreads through multiple interactive networks. This review discusses the increasingly well-understood mechanisms through which these enzymes alter chromatin function. In some cases at least, it seems that the effects on gene expression may persist even after the removal of the inducing agent, and can be passed on, through mitosis, to subsequent cell generations, constituting a heritable, epigenetic change. If such changes occur in germ cells or their precursors, then they may be passed on to subsequent generations. Mechanisms are now known to exist through which an epigenetic change might give rise to a localized change in DNA sequence exerting the same functional effect, thereby converting an epigenetic to a genetic change. If the induced genetic change has phenotypic effects on which selection can act, then this hypothetical chain of events constitutes a potential route through which the environment might directly influence evolution.

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Expression profile and estrogenic regulation of anti‐Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature‐dependent sex determination

Cited by 89 publications

References 29 publications

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

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

The effect of rearing temperature in larval development of pejerrey, Odontesthes bonariensis: morphological indicators of development

Epigenetic responses to environmental change and their evolutionary implications

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