Differential expression of reproduction and sex-determining genes in the gonads of genotypic and temperature-induced males of gibel carp (Carassius gibelio)

. 2025 Nov 25 ; 15 (1) : 43139. [epub] 20251125

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid41291041

Grantová podpora
22-27023S Czech Science Foundation

Odkazy

PubMed 41291041
PubMed Central PMC12678475
DOI 10.1038/s41598-025-27347-5
PII: 10.1038/s41598-025-27347-5
Knihovny.cz E-zdroje

Sex in vertebrates is commonly determined by genotype and environmental conditions, such as temperature. A few species display intermediate systems, combining sex chromosomes with temperature effect. This phenomenon has been reported in gibel carp (Carassius gibelio), an invasive cyprinid fish whose invasiveness is linked to the combination of sexual and asexual reproduction. Here, we compared gonadal transcriptomes between genotypic males and temperature-induced males of C. gibelio, focusing specifically on genes related to reproduction. Many meiosis and male differentiation pathways were common to genotypic and temperature-induced males. However, the underrepresentation of reproduction- and spermatogenesis-related terms in temperature-induced males suggests reduced reproductive abilities. Our study further highlights differential regulation of key genes related to male differentiation, steroid hormone signalling, meiosis, spermatogenesis, flagellar function, and sperm-egg interaction. In particular, induced males strongly overexpressed the key sex differentiation regulator hsd17b2 and slightly overexpressed the meiotic gene mnd1, while genotypic males overexpressed sox8a, cyp19a1a, and the crucial fertilization gene izumo. Our study highlights the importance of males in the transition from asexual to sexual reproduction in this species and contributes to understanding the molecular mechanisms underlying the reproductive plasticity and invasiveness of C. gibelio in Europe.

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Graves, J. A. M. Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. PubMed DOI

Bachtrog, D. et al. Sex determination: why so many ways of doing it? PubMed DOI PMC

Brown, E. E., Baumann, H. & Conover, D. O. Temperature and photoperiod effects on sex determination in a fish. DOI

Warner, R. R., Fitch, D. L. & Standish, J. D. Social control of sex change in the shelf limpet, DOI

Casas, L. et al. Sex change in clownfish: molecular insights from transcriptome analysis. PubMed DOI PMC

Shang, E. H. H., Yu, R. M. K. & Wu, R. S. S. Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish ( PubMed DOI

Baroiller, J. F., D’Cotta, H. & Saillant, E. Environmental effects on fish sex determination and differentiation. PubMed DOI

Robertson, C. E., Wright, P. A., Köblitz, L. & Bernier, N. J. Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, PubMed DOI PMC

Ospina-Álvarez, N. & Piferrer, F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PubMed DOI PMC

Conover, D. O., Van Voorhees, D. A. & Ehtisham, A. Sex ratio selection and the evolution of environmental sex determination in laboratory populations in PubMed DOI

Holleley, C. E. et al. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. PubMed DOI

Devlin, R. H. & Nagahama, Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. DOI

Wilson, C. A. et al. Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. PubMed DOI PMC

Sarre, S. D., Georges, A. & Quinn, A. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. PubMed DOI

Waters, P. D., Wallis, M. C. & Graves, J. A. M. Mammalian sex - origin and evolution of the Y chromosome and SRY. PubMed DOI

Schroeder, A. L., Metzger, K. J., Miller, A. & Rhen, T. A novel candidate gene for temperature-dependent sex determination in the common snapping turtle. PubMed DOI PMC

Matsuda, M. et al. PubMed DOI

Li, M. et al. A tandem duplicate of Anti-Müllerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile tilapia, PubMed DOI PMC

Chen, S. et al. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. PubMed DOI

Halačka, K., Lusková, V. & Lusk, S.

Lusková, V., Lusk, S., Halačka, K. & Vetešník, L. DOI

Perdikaris, C. et al. DOI

Wouters, J., Janson, S., Lusková, V. & Olsén, K. H. Molecular identification of hybrids of the invasive gibel carp PubMed DOI

Tapkir, S. et al. Invasive gibel carp ( DOI

Li, X. Y. et al. Evolutionary history of two divergent PubMed DOI

Luo, J. et al. Tempo and mode of recurrent polyploidization in the PubMed DOI PMC

Schlupp, I. The evolutionary ecology of gynogenesis. DOI

Neaves, W. B. & Baumann, P. Unisexual reproduction among vertebrates. PubMed DOI

Przybył, A. Sex, size and ploidy ratios of DOI

Ojima, Y. & Takai, A. Further cytogenetical studies on the origin of the goldfish. DOI

Li, X. Y. et al. Origin and transition of sex determination mechanisms in a gynogenetic hexaploid fish. PubMed DOI PMC

Goto-Kazeto, R. et al. Temperature-dependent sex differentiation in goldfish: Establishing the temperature-sensitive period and effect of constant and fluctuating water temperatures. DOI

Zhu, Y. J. et al. Distinct sperm nucleus behaviors between genotypic and temperature-dependent sex determination males are associated with replication and expression-related pathways in a gynogenetic fish. PubMed DOI PMC

Ahmad, S. F. & Martins, C. The modern view of B chromosomes under the impact of high scale omics analyses. PubMed DOI PMC

Ding, M. et al. Genomic anatomy of male-specific microchromosomes in a gynogenetic fish. PubMed DOI PMC

Li, X. Y. et al. Extra microchromosomes play male determination role in polyploid gibel carp. PubMed DOI PMC

Muller, H. J. The relation of recombination to mutational advance. PubMed DOI

Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites (a review). PubMed DOI PMC

Šimková, A., Košař, M., Vetešník, L. & Vyskočilová, M. MHC genes and parasitism in PubMed DOI PMC

Zhao, X. et al. Genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp. PubMed DOI PMC

Gui, J. & Zhou, L. Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid PubMed DOI

Du, W. X. et al. Gonadal temperature-sensitive gene identification in gynogenetic gibel carp ( DOI

Teng, J., Zhao, Y., Chen, H. J., Wang, H. & Ji, X. S. Transcriptome profiling and analysis of genes associated with high temperature-induced masculinization in sex-undifferentiated Nile tilapia gonad. PubMed DOI

Wang, C. et al. Comparative transcriptome analysis of heat-induced domesticated zebrafish during gonadal differentiation. PubMed DOI PMC

Brown-Peterson, N. J., Wyanski, D. M., Saborido‐Rey, F., Macewicz, B. J. & Lowerre‐Barbieri, S. K. A standardized terminology for describing reproductive development in fishes. DOI

Jacques, F. et al. Reproduction-associated pathways in females of gibel carp ( PubMed DOI PMC

Von Hofsten, J., Larsson, A. & Olsson, P. E. Novel steroidogenic factor-1 homolog ( PubMed DOI

Sandra, G. E. & Norma, M. M. Sexual determination and differentiation in teleost fish. DOI

Matsumoto, Y. & Crews, D. Molecular mechanisms of temperature-dependent sex determination in the context of ecological developmental biology. PubMed DOI

Hattori, R. S., Strüssmann, C. A., Fernandino, J. I. & Somoza, G. M. Genotypic sex determination in teleosts: insights from the testis-determining PubMed DOI

Merchant-Larios, H., Díaz-Hernández, V. & Cortez, D. Molecular and cellular mechanisms underlying temperature-dependent sex determination in turtles. PubMed DOI

Hillers, K. J. & Villeneuve, A. M. Chromosome-wide control of meiotic crossing over in PubMed DOI

Ramesh, M., Malik, S. & Logsdon, J. A. Phylogenomic inventory of meiotic genes evidence for sex in PubMed

Schurko, A. M. & Logsdon, J. M. Using a meiosis detection toolkit to investigate ancient asexual scandals and the evolution of sex. PubMed DOI

Patil, S. et al. Identification of the meiotic toolkit in diatoms and exploration of meiosis-specific PubMed DOI PMC

Maciver, S. K. Asexual amoebae escape muller’s ratchet through polyploidy. PubMed DOI

Kipreos, E. T. & Pagano, M. The F-box protein family. PubMed DOI PMC

Stacey, D. W. Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. PubMed DOI

Molina, J. R. & Adjei, A. A. The Ras/Raf/MAPK pathway. DOI

Tidyman, W. E. & Rauen, K. A. The rasopathies: developmental syndromes of Ras/MAPK pathway dysregulation. PubMed DOI PMC

Goriely, A. & Wilkie, A. O. M. Paternal age effect mutations and selfish spermatogonial selection: causes and consequences for human disease. PubMed DOI PMC

Birchmeier, C., Broek, D. & Wigler, M. RAS proteins can induce meiosis in xenopus oocytes. PubMed DOI

Cotton, L. M., O’Bryan, M. K. & Hinton, B. T. Cellular signaling by fibroblast growth factors (FGFs) and their receptors (FGFRs) in male reproduction. PubMed DOI PMC

Offen, N., Blum, N., Meyer, A. & Begemann, G. PubMed DOI PMC

Stenberg, P. & Saura, A. Meiosis and its deviations in polyploid animals. PubMed DOI

Spangenberg, V. et al. Reticulate evolution of the rock lizards: meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus PubMed DOI PMC

Hu, Y., Wang, B. & Du, H. A review on DOI

Han, J. et al. High temperature induced masculinization of zebrafish by down-regulation of PubMed DOI

Takada, S. & Koopman, P. Origin and possible roles of the PubMed DOI

Chaboissier, M. C. et al. Functional analysis of PubMed DOI

Yu, H. et al. The evolution and possible role of two PubMed DOI

Yang, B. et al. PubMed DOI

Yu, H. et al. Genome-wide identification and transcriptome-based expression analysis of Sox gene family in the Japanese flounder DOI

Barrionuevo, F. J. et al. PubMed DOI PMC

Xiao, L. et al. Comparative transcriptome analysis of diploid and triploid hybrid groupers ( PubMed DOI

Raymond, C. S., Kettlewell, J. R., Hirsch, B., Bardwell, V. J. & Zarkower, D. Expression of PubMed DOI

Marchand, O. et al. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, PubMed DOI

Ge, C. et al. PubMed

Poonlaphdecha, S. et al. Temperature induced-masculinisation in the Nile tilapia causes rapid up-regulation of both PubMed DOI

Fernandino, J. I., Hattori, R. S., Kimura, H., Strüssmann, C. A. & Somoza, G. M. Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey PubMed DOI

Shirak, A. et al. PubMed DOI PMC

Xu, S., Xia, W., Zohar, Y. & Gui, J. F. Zebrafish PubMed DOI

Yoshizawa, A. et al. Zebrafish Dmrta2 regulates neurogenesis in the telencephalon. PubMed DOI

Graf, M., Teo Qi-Wen, E.-R., Sarusie, M. V., Rajaei, F. & Winkler, C. Dmrt5 controls corticotrope and gonadotrope differentiation in the zebrafish pituitary. PubMed DOI PMC

Johnsen, H., Tveiten, H., Torgersen, J. S. & Andersen, Ø. Divergent and sex-dimorphic expression of the paralogs of the Sox9‐Amh‐Cyp19a1 regulatory cascade in developing and adult Atlantic cod ( PubMed DOI

Ahmed, S. Review of the molecular modelling studies of the cytochrome P-450 estrogen synthetase enzyme, aromatase. PubMed

Kitano, T., Takamune, K., Kobayashi, T., Nagahama, Y. & Abe, S. Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder ( PubMed DOI

D’Cotta, H., Fostier, A., Guiguen, Y., Govoroun, M. & Baroiller, J. Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia PubMed DOI

Ijiri, S. et al. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the nile tilapia PubMed DOI

Van Nes, S. & Andersen, Ø. Temperature effects on sex determination and ontogenetic gene expression of the aromatases PubMed DOI

Pfennig, F., Standke, A. & Gutzeit, H. O. The role of PubMed DOI

Rodríguez-Marí, A. et al. Characterization and expression pattern of zebrafish PubMed DOI

Johnsen, H. & Andersen, Ø. Sex dimorphic expression of five PubMed DOI

Wang, W. et al. PubMed DOI

Gomes Fernandes, M. et al. Human-specific subcellular compartmentalization of P-element induced wimpy testis-like (PIWIL) granules during germ cell development and spermatogenesis. PubMed DOI PMC

Manna, P. R., Stetson, C. L., Slominski, A. T. & Pruitt, K. Role of the steroidogenic acute regulatory protein in health and disease. PubMed DOI PMC

Deng, Q. et al. Sex-Inclined Piwi-Interacting RNAs in serum exosomes for sex determination in the greater amberjack ( PubMed DOI PMC

Giuili, G., Shen, W. H. & Ingraham, H. A. The nuclear receptor SF-1 mediates sexually dimorphic expression of Müllerian inhibiting substance, in vivo. PubMed DOI

Bollig, F. et al. Identification and comparative expression analysis of a second PubMed DOI

Valenzuela, N., Neuwald, J. L. & Literman, R. Transcriptional evolution underlying vertebrate sexual development. PubMed DOI

Zhou, T. et al. Single-molecule real-time sequencing for identifying sexual-dimorphism-related transcriptomes and genes in the Chinese soft-shelled turtle ( PubMed DOI PMC

Chen, R. et al. Characterization and functional analysis of the 17-beta hydroxysteroid dehydrogenase 2 ( PubMed DOI PMC

Erwin, D. H. The origin of animal body plans: a view from fossil evidence and the regulatory genome. PubMed DOI

Jacques, F., Baratchart, E., Pienta, K. J. & Hammarlund, E. U. Origin and evolution of animal multicellularity in the light of phylogenomics and cancer genetics. PubMed DOI PMC

Amberg, J. J., Goforth, R. R. & Sepúlveda, M. S. Antagonists to the Wnt cascade exhibit sex-specific expression in gonads of sexually mature shovelnose sturgeon. PubMed DOI

Liu, Y. et al. Sexually dimorphic expression in developing and adult gonads shows an important role of gonadal soma-derived factor during sex differentiation in olive flounder ( PubMed DOI

Prathibha, Y. & Senthilkumaran, B. Expression of PubMed DOI

Schiffer, M., Von Gersdorff, G., Bitzer, M., Susztak, K. & Böttinger, E. P. Smad proteins and transforming growth factor-β signaling. PubMed DOI

Aguero, T. et al. Hermes (Rbpms) is a critical component of RNP complexes that sequester germline RNAs during oogenesis. PubMed DOI PMC

Wilson, M. L. et al. Rbpms2 promotes female fate upstream of the nutrient sensing Gator2 complex component Mios. PubMed DOI PMC

Zhang, F. et al. Ski-related novel protein N (SnoN), a negative controller of transforming growth factor-beta signaling, is a prognostic marker in estrogen receptor-positive breast carcinomas. PubMed

Kobayashi, T. Involvement of gonadal soma-derived factor in the reproduction of teleosts. DOI

Shibata, Y. et al. Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. PubMed DOI

Horie, Y. et al. Androgen induces gonadal soma-derived factor, PubMed DOI

Kazama, H. et al. Loss of DIAPH3, a formin family protein, leads to cytokinetic failure only under high temperature conditions in mouse FM3A cells. PubMed DOI PMC

Xu, K. et al. Comparative analysis of testis transcriptomes from triploid and fertile diploid cyprinid fish. PubMed DOI

Pan, P. et al. Proteomic profiling of PubMed DOI

Li, D. Y. et al. Sperm flagellar 2 (SPEF2) is essential for sperm flagellar assembly in humans. PubMed DOI PMC

Grayson, P. Izumo1 and juno: the evolutionary origins and coevolution of essential sperm–egg binding partners. PubMed DOI PMC

Blobel, C. P. Functional processing of fertilin: evidence for a critical role of proteolysis in sperm maturation and activation. PubMed DOI

Ito, C. et al. Tetraspanin family protein CD9 in the mouse sperm: unique localization, appearance, behavior and fate during fertilization. PubMed DOI

Jacques, F., Bolivar, P., Pietras, K. & Hammarlund, E. U. Roadmap to the study of gene and protein phylogeny and evolution - a practical guide. PubMed DOI PMC

Dehler, C. E., Boudinot, P., Collet, B. & Martin, S. A. M. Phylogeny and expression of tetraspanin CD9 paralogues in rainbow trout ( PubMed DOI

Sebé-Pedrós, A., Roger, A. J., Lang, F. B., King, N. & Ruiz-Trillo, I. Ancient origin of the integrin-mediated adhesion and signaling machinery. PubMed DOI PMC

Merc, V., Frolikova, M. & Komrskova, K. Role of integrins in sperm activation and fertilization. PubMed DOI PMC

Wen, M. et al. Sex chromosome and sex locus characterization in goldfish, PubMed DOI PMC

Sperry, A. O. The dynamic cytoskeleton of the developing male germ cell. PubMed DOI PMC

Ma, D. D., Wang, D. H. & Yang W.-X. Kinesins in spermatogenesis. PubMed DOI

Sun, M., Li, Z. & Gui, J. Dynamic distribution of Spindlin in nucleoli, nucleoplasm and spindle from primary oocytes to mature eggs and its critical function for oocyte-to‐embryo transition in gibel carp. PubMed DOI

Kuhl, H. et al. Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp. PubMed DOI PMC

Yuan, J. et al. Speciation of polyploid Cyprinidae fish of common carp, crucian carp, and silver crucian carp derived from duplicated PubMed DOI

Zhou, L., Wang, Y. & Gui, J. F. Genetic evidence for gonochoristic reproduction in gynogenetic silver crucian carp ( PubMed DOI

Šimková, A., Dávidová, M., Papoušek, I. & Vetešník, L. Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? PubMed DOI PMC

Pakosta, T., Vetešník, L. & Šimková, A. Long temporal study of parasitism in asexual-sexual populations of PubMed DOI PMC

Fuad, M. M. H., Vetešník, L. & Šimková, A. Is gynogenetic reproduction in gibel carp ( DOI

Šimková, A., Vojtek, L., Halačka, K., Hyršl, P. & Vetešník, L. The effect of hybridization on fish physiology, immunity and blood biochemistry: a case study in hybridizing DOI

Papoušek, I. et al. Identification of natural hybrids of gibel carp DOI

Gela, D. et al. Controlled reproduction technology of common carp (

Suvarna, K. S., Layton, C. & Bancroft, J. D.

Andrews, S. FastQC: a quality control tool for high throughput sequence data. (2010).

Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. PubMed DOI PMC

Wang, L., Wang, S. & Li, W. RSeQC: quality control of RNA-seq experiments. PubMed DOI

Picard Toolkit. Broad Institute. (2018).

Okonechnikov, K., Conesa, A. & García-Alcalde, F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. PubMed DOI PMC

Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. PubMed DOI PMC

Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. PubMed DOI

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Ge, S. X., Son, E. W. & Yao, R. iDEP: an integrated web application for differential expression and pathway analysis of RNA-Seq data. PubMed DOI PMC

The Gene Ontology Consortium. The gene ontology resource: enriching a gold mine. PubMed PMC

Kanehisa, M. & Goto, S. K. E. G. G. Kyoto encyclopedia of genes and genomes. PubMed DOI PMC

Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. PubMed DOI PMC

Kanehisa, M., Furumichi, M., Sato, Y., Matsuura, Y. & Ishiguro-Watanabe, M. KEGG: biological systems database as a model of the real world. PubMed DOI PMC

Sherman, B. T. et al. DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). PubMed DOI PMC

Bairoch, A. The universal protein resource (UniProt). PubMed DOI PMC

Bradford, Y. M. et al. Zebrafish information network, the knowledgebase for PubMed DOI PMC

Safran, M. et al. GeneCards Version 3: the human gene integrator. Database baq020–baq020 (2010). (2010). PubMed PMC

Schedina, I. M., Groth, D., Schlupp, I. & Tiedemann, R. The gonadal transcriptome of the unisexual Amazon molly PubMed DOI PMC

Vandesompele, J., Preter, K. D., Roy, N. V. & Paepe, A. D. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. PubMed PMC

Ye, J. et al. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. PubMed DOI PMC

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 PubMed DOI

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