Genetic regulation of sex determination and gonadal differentiation in teleost fish
DOI:
https://doi.org/10.18041/1900-3803/entramado.1.7607Keywords:
Aquaculture species, Gene expression, Sex determination, Neotropical fish, Sex chromosome, Sexual plasticityAbstract
Understanding the control in the determination and differentiation of sex in fish is essential to improve aspects of management, productivity, economy and conservation of the species. The objective of this review is to provide information on the main genetic-molecular mechanisms of sexual determination and differentiation in teleost fish. The information search was developed between 2019 - 2021 through bibliographic databases using phrases such as: "sex determination fish", "sexual differentiation fish" and "sex neotropical fish". The selection of the information was carried out taking into consideration a maximum of 10 years of publication, discarding documents considered as master's or doctoral theses. The sex determination can be defined by chromosome systems such as XX/XY, ZZ/ZW, XX/X0, ZZ/Z0, XX1, XX2 and X1X2Y or modulated by different autosomal genes such as cyp19a1, foxl2, figla, dmrt1, sox9, amh, gsdf. However, despite the great advances in research in the molecular area, the regulation process in the determination and differentiation of sex in fish is not yet fully elucidated, especially in species Neotropical.
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ANITHA, A.; GUPTA, Y.-R.; DEEPA, S.; NINGAPPA, M.; RAJANNA, K. B.; SENTHILKUMARAN, B. Gonadal transcriptome analysis of the common carp, Cyprinus carpio: Identification of differentially expressed genes and SSRs. In: General and Comparative Endocrinology. 2019. vol. 279. p. 67-77. https://doi.org/10.1016/J.YGCEN.2018.12.004
AROSTEGUI, M. C.; QUINN, T. P.; SEEB, L. W.; SEEB, J. E.; MCKINNEY, G. J. Retention of a chromosomal inversion from an anadromous ancestor provides the genetic basis for alternative freshwater ecotypes in rainbow trout. In: Molecular Ecology. 2019. https://doi.org/10.1111/mec.15037
BAHAMONDE, P. A.; MUNKITTRICK, K. R.; MARTYNIUK, C. J. Intersex in teleost fish: Are we distinguishing endocrine disruption from natural phenomena? In: General and Comparative Endocrinology. 2013. vol. 192. p. 25-35. https://doi.org/10.1016/J.YGCEN.2013.04.005
BANH, Q. Q.; DOMINGOS, J. A.; ZENGER, K. R.; JERRY, D. R. Morphological changes and regulation of the genes dmrt1 and cyp11b during the sex differentiation of barramundi (Lates calcarifer Bloch). In: Aquaculture. 2017. vol. 479. p. 75-84. https://doi.org/10.1016/J.AQUACULTURE.2017.05.022
BHANDARI, R. K.; NAKAMURA, M.; KOBAYASHI, T.; NAGAHAMA, Y. Suppression of steroidogenic enzyme expression during androgen-induced sex reversal in Nile tilapia (Oreochromis niloticus). In: General and Comparative Endocrinology. 2006. vol. 145(1). p. 20-24. https://doi.org/10.1016/J.YGCEN.2005.06.014
BURGOS-ACEVES, M. A.; COHEN, A.; SMITH, Y.; FAGGIO, C. Estrogen regulation of gene expression in the teleost fish immune system. In: Fish & Shellfish Immunology. 2016. vol. 58. p. 42-49. https://doi.org/10.1016/J.FSI.2016.09.006
CRESPO, B.; LAN-CHOW-WING, O.; ROCHA, A.; ZANUY, S.; GÓMEZ, A. foxl2 and foxl3 are two ancient paralogs that remain fully functional in teleosts. In: General and Comparative Endocrinology. 2013. vol. 194. p. 81-93. https://doi.org/10.1016/J.YGCEN.2013.08.016
DE SIQUEIRA-SILVA, D. H.; DA SILVA RODRIGUES, M.; NÓBREGA, R. H. Testis structure, spermatogonial niche and Sertoli cell efficiency in Neotropical fish. In: General and Comparative Endocrinology. 2019. vol. 273. p. 218-226. https://doi.org/10.1016/J.YGCEN.2018.09.004
DEVLIN, R. H.; NAGAHAMA, Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. In: Aquaculture. 2002. vol. 208(3-4). p. 191-364. https://doi.org/10.1016/S0044-8486(02)00057-1
DIOTEL, N.; PAGE, Y. LE.; MOURIEC, K.; TONG, S.-K.; PELLEGRINI, E.; VAILLANT, C.; ANGLADE, I.; BRION, F.; PAKDEL, F.; CHUNG, B.; KAH, O. Aromatase in the brain of teleost fish: Expression, regulation and putative functions. In: Frontiers in Neuroendocrinology. 2010. vol. 31(2). p. 172-192. https://doi.org/10.1016/J.YFRNE.2010.01.003
FERNANDINO, J. I.; HATTORI, R. S. Sex determination in Neotropical fish: Implications ranging from aquaculture technology to ecological assessment. In: General and Comparative Endocrinology. 2019. vol. 273. p. 172-183. https://doi.org/10.1016/J.YGCEN.2018.07.002
FOWLER, B. L. S.; BUONACCORSI, V. P. Genomic characterization of sex-identification markers in Sebastes carnatus and Sebastes chrysomelas rockfishes. In: Molecular Ecology. 2016. vol. 25. p. 2165-2175. https://doi.org/doi: 10.1111/mec.13594
GALETTI, P. M.; FORESTI, F.; BERTOLLO, L. A. C.; MOREIRA FILHO, O. Karyotypic similarity in three genera (Leporinus, Leporellus, Schizodon) of the family Anostomidae (Pisces, Teleostei). In: Brazil J Genet. 1981. vol. 4.
GAVERY, M. R.; NICHOLS, K. M.; GOETZ, G. W.; MIDDLETON, M. A.; SWANSON, P. Characterization of genetic and epigenetic variation in sperm and red blood cells from adult hatchery and natural-origin steelhead, Oncorhynchus mykiss. In: G3: Genes, Genomes, Genetics. 2018. https://doi.org/10.1534/g3.118.200458
GEMMELL, N. J.; TODD, E. V.; GOIKOETXEA, A.; ORTEGA-RECALDE, O.; HORE, T. A. Natural sex change in fish. In: Current Topics in Developmental Biology. 2019. vol. 134. p. 71-117. https://doi.org/10.1016/BS.CTDB.2018.12.014
GONZALEZ, J. A.; BUENO, M. L.; FORERO, J. E. Caracterización cromosómica de dos especies icticas nativas; guapucha, (Grundulus bogotensis) y capitan, (Eremophilus mutisii), de la sabana de Bogotá. En: Acta Biológica Colombiana. 1992. vol. 2(7). p. 45-54. https://doi.org/10.15446/abc
GRÖNER, F.; HÖHNE, C.; KLEINER, W.; KLOAS, W. Chronic diclofenac exposure affects gill integrity and pituitary gene expression and displays estrogenic activity in nile tilapia (Oreochromis niloticus). In: Chemosphere. 2017. https://doi.org/10.1016/j.chemosphere.2016.09.116
HENNING, F.; MOYSÉS, C. B.; CALCAGNOTTO, D.; MEYER, A.; ALMEIDA-TOLEDO, L. F. Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia). In: Heredity. 2011. vol. 106. https://doi.org/10.1038/hdy.2010.82
HU, Q.; XIAO, H.; TIAN, H.; MENG, Y. Identification and expression of cytochrome P450 genes in the Chinese giant salamander Andrias davidianus. In: Theriogenology. 2017. vol. 95. p. 62-68. https://doi.org/10.1016/J.THERIOGENOLOGY.2017.03.001
JENG, S.-R.; WU, G.-C.; YUEH, W.-S.; KUO, S.-F.; DUFOUR, S.; CHANG, C.-F.. Gonadal development and expression of sex-specific genes during sex differentiation in the Japanese eel. In: General and Comparative Endocrinology. 2018. vol. 257, p. 74-85. https://doi.org/10.1016/J.YGCEN.2017.07.031
JIN, Y. H.; DAVIE, A.; MIGAUD, H. Expression pattern of nanos, piwil, dnd, vasa and pum genes during ontogenic development in Nile tilapia Oreochromis niloticus. In: Gene. 2019. vol. 688. p. 62–70. https://doi.org/10.1016/J.GENE.2018.11.078
LI, H.; XU, W.; ZHANG, N.; SHAO, C.; ZHU, Y.; DONG, Z.; WANG, N.; JIA, X.; XU, H.; CHEN, S. Two Figla homologues have disparate functions during sex differentiation in half-smooth tongue sole (Cynoglossus semilaevis). In: Scientific Reports. 2016. vol. 6, p. 28219. https://doi.org/10.1038/srep28219
LI, M; WANG, D. (2017). Gene editing nuclease and its application in tilapia. In: Science Bulletin. 2017. vol. 62(3). p. 165-173. https://doi.org/10.1016/J.SCIB.2017.01.003
LI, Meng; WANG, L.; WANG, H.; LIANG, H.; ZHENG, Y.; QIN, F.; LIU, S.; ZHANG, Y.; WANG, Z. Molecular cloning and characterization of amh, dax1 and cyp19a1a genes and their response to 17α-methyltestosterone in Pengze crucian carp. In: Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2013. vol. 157(4). p. 372-381. https://doi.org/10.1016/J.CBPC.2013.03.005
LIN, Q.; HE, Y.; GUI, J. F.; MEI, J. Sox9a, not sox9b is required for normal cartilage development in zebrafish. In: Aquaculture and Fisheries. 2021. vol. 6(3). p. 254-259. https://doi.org/10.1016/j.aaf.2019.12.009
MAROSO, F.; HERMIDA, M.; MILLÁN, A.; BLANCO, A.; SAURA, M.; FERNÁNDEZ, A.; DALLA ROVERE, G.; BARGELLONI, L.; CABALEIRO, S.; VILLANUEVA, B., BOUZA, C.; MARTÍNEZ, P. Highly dense linkage maps from 31 full-sibling families of turbot (Scophthalmus maximus) provide insights into recombination patterns and chromosome rearrangements throughout a newly refined genome assembly. In: DNA Research. 2018. https://doi.org/10.1093/dnares/dsy015
MARQUIONI, V.; BERTOLLO, L. A. C.; DINIZ, D.; CIOFFI, M. DE B. Comparative chromosomal mapping in Triportheus fish species. Analysis of synteny between ribosomal genes. In: Micron. 2013. vol. 45. p. 129-135. https://doi.org/10.1016/J.MICRON.2012.11.008
MARTÍNEZ, P.; VIÑAS, A. M.; SÁNCHEZ, L.; DÍAZ, N.; RIBAS, L.; PIFERRER, F. Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture. In: Frontiers in Genetics. 2014. vol. 5. p. 340. https://doi.org/10.3389/fgene.2014.00340
MIYAKE, Y.; SAKAI, Y.; KUNIYOSHI, H. Molecular Cloning and Expression Profile of Sex-Specific Genes, Figla and Dmrt1, in the Protogynous Hermaphroditic Fish, Halichoeres Poecilopterus. In: Zoological Science. 2012. vol. 29(10). p. 690-710. https://doi.org/10.2108/zsj.29.690
MOJICA, J. I.; USMA, J. S.; ÁLVAREZ-LEÓN, R.; LASSO, C. A. Libro Rojo de peces dulceacuícolas de Colombia (J. I. Mojica, J. S. Usma, R. Álvarez-León, & C. A. Lasso (eds.)). Instituto de Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Instituto de Ciencias Naturales de la Universidad Nacional de Colombia, WWF Colombia y Universidad de Manizales. 2012. http://awsassets.panda.org/downloads/libro_rojo_peces_dulceacuicolas_de_colombia___dic_2012.pdf
MOORE, E. C.; ROBERTS, R. B. Polygenic sex determination. In: Current Biology. 2013. vol. 23(12). p R510-2. https://doi.org/10.1016/j.cub.2013.04.004
OKADA, H.; HAGIHARA, S.; YAMASHITA, K.; IJIRI, S.; ADACHI, S. (2017). Expression pattern of foxl2 and dmrt1 in gonad of Amur sturgeon Acipenser schrenckii in relation to sex differentiation. In: Aquaculture. 2017. vol. 479. p. 712-720. https://doi.org/10.1016/J.AQUACULTURE.2017.07.020
OKUBO, K.; MIYAZOE, D.; NISHIIKE, Y. A conceptual framework for understanding sexual differentiation of the teleost brain. In: General and Comparative Endocrinology. 2019. https://doi.org/10.1016/J.YGCEN.2019.02.020
PAN, Q.; GUIGUEN, Y.; HERPIN, A. Evolution of Sex Determining Genes in Fish. In: Encyclopedia of Reproduction. 2018. p. 168-175. https://doi.org/10.1016/B978-0-12-809633-8.20552-9
PÉREZ, C.; ARANEDA, C.; ESTAY, F.; DÍAZ, N. F.; VIZZIANO-CANTONNET, D. Sex hormone-binding globulin b expression in the rainbow trout ovary prior to sex differentiation. In: General and Comparative Endocrinology. 2018. vol. 259. p. 165-175. https://doi.org/10.1016/J.YGCEN.2017.11.021
PIFERRER, F. Endocrine sex control strategies for the feminization of teleost fish. In: Aquaculture. 2001. vol. 197(1-4). p. 229-281. https://doi.org/10.1016/S0044-8486(01)00589-0
PIFERRER, F. (2013). Epigenetics of sex determination and gonadogenesis. In: Developmental Dynamics. 2013. vol. 242(4). https://doi.org/10.1002/dvdy.23924
PRIETO-MOJICA, C.; GALLEGO-ALARCÓN, F.; MONCALEANO GÓMEZ, E. (2017). Pez Capitan de La Sabana (Eremophilus mutisii). En: Zoociencia. 2017. vol. 4(2). p. 4-9.
RAMALLO, M. R.; MORANDINI, L.; BIRBA, A.; SOMOZA, G. M.; PANDOLFI, M. (2017). From molecule to behavior: Brain aromatase (cyp19a1b) characterization, expression analysis and its relation with social status and male agonistic behavior in a Neotropical cichlid fish. In: Hormones and Behavior. 2017. vol. 89, p. 176-188. https://doi.org/10.1016/J.YHBEH.2017.02.005
REYHANIAN CASPILLO, N.; VOLKOVA, K.; HALLGREN, S.; OLSSON, P. E.; PORSCH-HÄLLSTRÖM, I. Short-term treatment of adult male zebrafish (Danio Rerio) with 17α-ethinyl estradiol affects the transcription of genes involved in development and male sex differentiation. In: Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology. 2014. https://doi.org/10.1016/j.cbpc.2014.04.003
RIBAS, L.; ROBLEDO, D.; GÓMEZ-TATO, A.; VIÑAS, A.; MARTÍNEZ, P.; PIFERRER, F. Comprehensive transcriptomic analysis of the process of gonadal sex differentiation in the turbot (Scophthalmus maximus). In: Molecular and Cellular Endocrinology. 2016. vol. 422. https://doi.org/10.1016/j.mce.2015.11.006
RODRIGUES, M.; CALABUIG, C.; ÃVILA MOREIRA, C.; CAMACHO DA SILVA, J.; BENDER ALMEIDA, D.; PEREZ GUTIERREZ, H.; MARQUES MOREIRA, H. The expression of CYP19a gene at two temperature levels during the thermosensitive period of the Nile Tilapia (Oreochromis niloticus). In: Animal Molecular Breeding. 2015. vol. 5(2). p. 1-6. https://doi.org/10.5376/amb.2015.05.0002
RODRÍGUEZ-PULIDO, J.; MIRA-LÓPEZ, T.; CRUZ-CASALLAS, P. Determinación, diferenciación sexual y pubertad en peces. En: ORINOQUIA - Universidad de Los Llanos - Villavicencio Meta. 2018. vol. 22. p. 80-91.
ROUGEOT, C.; PRIGNON, C.; NGOUANA KENGNE, C. V.; MÉLARD, C. Effect of high temperature during embryogenesis on the sex differentiation process in the Nile tilapia, Oreochromis niloticus. In: Aquaculture. 2008. vol. 276(1-4). p. 205-208. https://doi.org/10.1016/J.AQUACULTURE.2008.02.001
SALAME-MÉNDEZ, A.; VILLALPANDO-FIERRO, I. La diferenciación sexual en vertebrados hipótesis y teorías. En: Acta Zoológica Mexicana (Nueva Serie). 1998. vol. 73.
SANTI, S.; GENNOTTE, V.; MULLER, M.; MELARD, C.; TOGUYENI, A.; MANDIKI, S. N. M.; ROUGEOT, C. Sex-ratio, early sex steroid profiles and cyp19a1b, dmrt1 and foxl2 gene expressions upon high temperature treatment of undifferentiated African catfish juveniles (Clarias gariepinus). In: Aquaculture. 2019. vol. 499. p. 140-148. https://doi.org/10.1016/J.AQUACULTURE.2018.09.033
SIEGFRIED, K. R. Molecular and Chromosomal Aspects of Sex Determination. In: Reference Module in Life Sciences. 2017. https://doi.org/10.1016/B978-0-12-809633-8.03245-3
SILVA, E. L.; BORBA, R. S.; PARISE-MALTEMPI, P. P. Chromosome mapping of repetitive sequences in Anostomidae species: implications for genomic and sex chromosome evolution. In: Molecular Cytogenetics. 2012. vol. 5. https://doi.org/10.1186/1755-8166-5-45
SINGH, A. K. Introduction of modern endocrine techniques for the production of monosex population of fishes. In: General and Comparative Endocrinology. 2013. vol. 181. p. 146-155. https://doi.org/10.1016/J.YGCEN.2012.08.027
TESSEMA, M.; MÜLLER-BELECKE, A.; HÖRSTGEN-SCHWARK, G. Effect of rearing temperatures on the sex ratios of Oreochromis niloticus populations. In: Aquaculture. 2006. vol. 258(1-4). p. 270-277. https://doi.org/10.1016/J.AQUACULTURE.2006.04.041
TOKARZ, J.; MÖLLER, G.; HRABĚ DE ANGELIS, M.; ADAMSKI, J. Steroids in teleost fishes: A functional point of view. In: Steroids. 2015. vol. 103. p. 123-144. https://doi.org/10.1016/J.STEROIDS.2015.06.011
TRUKHINA, A. V.; LUKINA, N. A.; WACKEROW-KOUZOVA, N. D.; SMIRNOV, A. F. The variety of vertebrate mechanisms of sex determination. In: BioMed Research International. 2013. vol. 2013. https://doi.org/10.1155/2013/587460
VALDELAMAR-VILLEGAS, J. (2018). Apuntes sobre la importancia ecológica, ambiental y social de la arenca Triportheus magdalenae (Steindachner, 1878). Un ejemplo de endemismo invisibilizado. En: Intropica, Julio-Diciembre 2018. https://doi.org/http://dx.doi.org/10.21676/23897864.2628
VICARI, M. R.; ARTONI, R. F.; MOREIRA-FILHO, O.; BERTOLLO, L. A. C. Diversification of a ZZ/ ZW sex chromosome system in Characidium fish (Crenuchidae, Characiformes). In: Genetica. 2008. vol. 134 (3). p. 311-317. https://doi.org/10.1007/s10709-007-9238-2
VICARI, Marcelo Ricardo, FERREIRA ARTONI, R.; MOREIRA-FILHO, O.; BERTOLLO, L. A. C. Diversification of a ZZ/ZW sex chromosome system in Characidium fish (Crenuchidae, Characiformes). In: Genetica. 2008. vol. 147(388). p. 134:311. https://doi.org/https://doi.org/10.1007/s10709-007-9238-2
WANG, H.-P.; PIFERRER, F.; CHEN, S.L. Sex Control in Aquaculture (H.-P. Wang, F. Piferrer, & S. Chen (eds.). 2019. Vol. 1). Jhon Wiley & Sons Ltd.
WEBSTER, K. A.; SCHACH, U.; ORDAZ, A.; STEINFELD, J. S.; DRAPER, B. W.; SIEGFRIED, K. R. Dmrt1 is necessary for male sexual development in zebrafish. In: Developmental Biology. 2017. vol. 422(1). p. 33-46. https://doi.org/10.1016/J.YDBIO.2016.12.008
WEI, L.; LI, X.; LI, M.; TANG, Y.; WEI, J.; WANG, D. Dmrt1 directly regulates the transcription of the testis-biased Sox9b gene in Nile tilapia (Oreochromis niloticus). In: Gene. 2019. vol. 687. p. 109-115. https://doi.org/10.1016/J.GENE.2018.11.016
YAMAMOTO, Y.; HATTORI, R. S.; PATIÑO, R.; STRÜSSMANN, C. A. Environmental regulation of sex determination in fishes: Insights from Atheriniformes. In: Current Topics in Developmental Biology. 2019. vol. 134. p. 49-69. https://doi.org/10.1016/BS.CTDB.2019.02.003
YU, X.; WU, L.; XIE, L.; YANG, S.; CHARKRABORTY, T.; SHI, H.; WANG, D.; ZHOU, L. Characterization of two paralogous StAR genes in a teleost, Nile tilapia (Oreochromis niloticus). In: Molecular and Cellular Endocrinology. 2014. vol. 392(1-2). p. 152-162. https://doi.org/10.1016/J.MCE.2014.05.013
ZHANG, S.; ZHANG, X.; CHEN, X.; XU, T.; WANG, M.; QIN, Q.; ZHONG, L.; JIANG, H.; ZHU, X.; LIU, H.; SHAO, J.; ZHU, Z.; SHI, Q.; BIAN, W.; YOU, X. Construction of a high-density linkage map and QTL fine mapping for growth- And sex-related traits in channel catfish (Ictalurus punctatus). In: Frontiers in Genetics. 2019. vol. 10. 14p. https://doi.org/10.3389/fgene.2019.00251
ZHANG, Y.; ZHANG, S.; LU, H.; ZHANG, L.; ZHANG, W. Genes encoding aromatases in teleosts: Evolution and expression regulation. In: General and Comparative Endocrinology. 2014. vol. 205. p. 151-158. https://doi.org/10.1016/J.YGCEN.2014.05.008
ZHOU, L.; LUO, F.; FANG, X.; CHARKRABORTY, T.; WU, L.; WEI, J.; WANG, D. Blockage of progestin physiology disrupts ovarian differentiation in XX Nile tilapia (Oreochromis niloticus). In: Biochemical and Biophysical Research Communications. 2016. vol. 473(1). p. 29-34. https://doi.org/10.1016/J.BBRC.2016.03.045
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