A chromosome-level genome assembly enables the identification of the follicule stimulating hormone receptor as the master sex-determining gene in the flatfish Solea senegalensis.
Senegalese sole
follicule stimulating hormone receptor
genetic map
sex determination
whole genome sequencing
Journal
Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
revised:
23
12
2022
received:
01
08
2022
accepted:
28
12
2022
medline:
6
4
2023
pubmed:
2
1
2023
entrez:
1
1
2023
Statut:
ppublish
Résumé
Sex determination (SD) shows huge variation among fish and a high evolutionary rate, as illustrated by the Pleuronectiformes (flatfishes). This order is characterized by its adaptation to demersal life, compact genomes and diversity of SD mechanisms. Here, we assembled the Solea senegalensis genome, a flatfish of great commercial value, into 82 contigs (614 Mb) combining long- and short-read sequencing, which were next scaffolded using a highly dense genetic map (28,838 markers, 21 linkage groups), representing 98.9% of the assembly. Further, we established the correspondence between the assembly and the 21 chromosomes by using BAC-FISH. Whole genome resequencing of six males and six females enabled the identification of 41 single nucleotide polymorphism variants in the follicle stimulating hormone receptor (fshr) consistent with an XX/XY SD system. The observed sex association was validated in a broader independent sample, providing a novel molecular sexing tool. The fshr gene displayed differential expression between male and female gonads from 86 days post-fertilization, when the gonad is still an undifferentiated primordium, concomitant with the activation of amh and cyp19a1a, testis and ovary marker genes, respectively, in males and females. The Y-linked fshr allele, which included 24 nonsynonymous variants and showed a highly divergent 3D protein structure, was overexpressed in males compared to the X-linked allele at all stages of gonadal differentiation. We hypothesize a mechanism hampering the action of the follicle stimulating hormone driving the undifferentiated gonad toward testis.
Identifiants
pubmed: 36587276
doi: 10.1111/1755-0998.13750
doi:
Substances chimiques
Receptors, FSH
0
Hormones
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
886-904Subventions
Organisme : European Union's Horizon 2020 research and innovation programme under grant agreement (AQUA-FAANG)
ID : 81792
Organisme : Junta de Andalucía-FEDER Grant
ID : P20-00938
Organisme : Spanish Ministry of Economy and Competitiveness, FEDER Grants
ID : RTI2018-096847-B-C21
Organisme : Spanish Ministry of Economy and Competitiveness, FEDER Grants
ID : RTI2018-096847-B-C22
Organisme : Ministry of Economy and Competitiveness
Organisme : Junta de Andalucía
Organisme : European Union
Organisme : Horizon 2020
Informations de copyright
© 2023 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.
Références
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
Baek, M., DiMaio, F., Anishchenko, I., Dauparas, J., Ovchinnikov, S., Lee, G. R., Wang, J., Cong, Q., Kinch, L. N., Schaeffer, R. D., Millán, C., Park, H., Adams, C., Glassman, C. R., DeGiovanni, A., Pereira, J. H., Rodrigues, A. V., van Dijk, A. A., Ebrecht, A. C., … Baker, D. (2021). Accurate prediction of protein structures and interactions using a three-track neural network. Science, 373, 871-876. https://doi.org/10.1126/science.abj8754
Bao, L., Tian, C., Liu, S., Zhang, Y., Elaswad, A., Yuan, Z., Khalil, K., Sun, F., Yang, Y., Zhou, T., Li, N., Tan, S., Zeng, Q., Liu, Y., Li, Y., Li, Y., Gao, D., Dunham, R., Davis, K., … Liu, Z. (2019). The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish. BMC Biology, 17, 6. https://doi.org/10.1186/s12915-019-0627-7
Buchfink, B., Reuter, K., & Drost, H. G. (2021). Sensitive protein alignments at tree-of-life scale using DIAMOND. Nature Methods, 18, 366-368. https://doi.org/10.1038/s41592-021-01101-x
Cabral, H. N. (2000). Comparative feeding ecology of sympatric Solea solea and Solea senegalensis, within nursery areas of the Tagus estuary, Portugal. Journal of Fish Biology, 57, 1550-1562. https://doi.org/10.1111/j.1095-8649.2000.tb02231.x
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22, 3124-3140.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2020). Chromonomer: A tool set for repairing and enhancing assembled genomes through integration of genetic maps and conserved synteny. G3- Genes Genomes Genetics, 10, 4115-4128.
Chen, S., Zhang, G., Shao, C., Huang, Q., Liu, G., Zhang, P., Song, W., An, N., Chalopin, D., Volff, J. N., Hong, Y., Li, Q., Sha, Z., Zhou, H., Xie, M., Yu, Q., Liu, Y., Xiang, H., Wang, N., … Wang, J. (2014). Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nature Genetics, 46, 253-260. https://doi.org/10.1038/ng.2890
Chen, S., Zhou, Y., Chen, Y., & Gu, J. (2018). fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884-i890. https://doi.org/10.1093/bioinformatics/bty560
Cioffi, M. B., Yano, C. F., Sember, A., & Bertollo, L. A. C. (2017). Chromosomal evolution in lower vertebrates: Sex chromosomes in Neotropical fishes. Genes, 8, 258. https://doi.org/10.3390/genes8100258
Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M., & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676. https://doi.org/10.1093/bioinformatics/bti610
Cui, X., Lu, Z., Wang, S., Wang, J. J.-Y., & Gao, X. (2016). CMsearch: Simultaneous exploration of protein sequence space and structure space improves not only protein homology detection but also protein structure prediction. Bioinformatics, 32, i332-i340. https://doi.org/10.1093/bioinformatics/btw271
Curzon, A. Y., Dor, L., Shirak, A., Meiri-Ashkenazi, I., Rosenfeld, H., Ron, M., & Seroussi, E. (2021). A novel c.1759T>G variant in follicle-stimulating hormone-receptor gene is concordant with male determination in the flathead grey mullet (Mugil cephalus). G3-Genes Genomes Genetics, 11, jkaa044. https://doi.org/10.1093/g3journal/jkaa044
de la Herrán, R., Hermida, M., Rubiolo, J., Gómez-Garrido, J., Cruz, F., Robles, F., Navajas-Pérez, R., Blanco, A., Villamayor, P. R., Torres, D., Sanchez-Quinteiro, P., & Ramirez, D. (2022). A chromosome-level genome assembly enables the identification of the follicle stimulating hormone receptor as the master sex determining gene in Solea senegalensis. bioRvix. https://doi.org/10.1101/2022.03.02.482245
Díaz-Ferguson, E., Cross, I., Barrios, M., Pino, A., Castro, J., Bouza, C., Martínez, P., & Rebordinos, L. (2012). Genetic characterization, based on microsatellite loci, of Solea senegalensis (Soleidae, Pleuronectiformes) in Atlantic coast populations of the SW Iberian Peninsul. Ciencias Marinas, 38, 129-142.
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013). STAR: ultrafast universal RNA-Seq aligner. Bioinformatics, 29, 15-21. https://doi.org/10.1093/bioinformatics/bts635
Drinan, D. P., Loher, T., & Hauser, L. (2018). Identification of genomic regions associated with sex in Pacific halibut. Journal of Heredity, 109, 326-332. https://doi.org/10.1093/jhered/esx102
Edvardsen, R. B., Wallerman, O., Furmanek, T., Kleppe, L., Jern, P., Wallberg, A., Kjaerner-Semb, E., Maehle, S., Olausson, S. K., Sundström, E., Harboe, T., Mangor-Jensen, R., Møgster, M., Perrichon, P., Norberg, B., & Rubin, C. J. (2022). Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut. PLoS Genetics, 8(18), e1010011. https://doi.org/10.1371/journal.pgen.1010011
Einfeldt, A. L., Kess, T., Messmer, A., Duffy, S., Wringe, B. F., Fisher, J., den Heyer, C., Bradbury, I. R., Ruzzante, D. E., & Bentzen, P. (2021). Chromosome level reference of Atlantic halibut Hippoglossus hippoglossus provides insight into the evolution of sexual determination systems. Molecular Ecology Resources, 21, 1686-1696. https://doi.org/10.1111/1755-0998.13369
Erdös, G., Pajkos, M., & Dosztányi, Z. (2021). IUPred3: Prediction of protein disorder enhanced with unambiguous experimental annotation and visualization of evolutionary conservation. Nucleic Acids Research, 49, W297-W303. https://doi.org/10.1093/nar/gkab408
Ferchaud, A. L., Mérot, C., Normandeau, E., Ragoussis, J., Babin, C., Djambazian, H., Bérubé, P., Audet, C., Treble, M., Walkusz, W., & Bernatchez, L. (2022). Chromosome-level assembly reveals a putative Y-autosomal fusion in the sex determination system of the Greenland halibut (Reinhardtius hippoglossoides). G3- Genes Genomes Genetics, 12, jkab376. https://doi.org/10.1093/g3journal/jkab376
Feron, R., Zahm, M., Cabaum, C., Klopp, C., Roques, C., Bouchez, O., Eché, C., Valière, S., Donnadieu, C., Haffray, P., & Bestin, A. (2020). Characterization of a Y-specific duplication/insertion of the anti-Mullerian hormone type II receptor gene based on a chromosome-scale genome assembly of yellow perch, Perca flavescens. Molecular Ecology Resources, 20, 531-543. https://doi.org/10.1111/1755-0998.13133
Ferraresso, S., Bargelloni, L., Babbucci, M., Cannas, R., Follesa, M. C., Carugati, L., Melis, R., Cau, A., Koutrakis, M., Sapounidis, A., Crosetti, D., & Patarnello, T. (2021). Fshr: A fish sex-determining locus shows variable incomplete penetrance across flathead grey mullet populations. iScience, 24, 101886. https://doi.org/10.1016/j.isci.2020.101886
Figueras, A., Robledo, D., Corvelo, A., Hermida, M., Pereiro, P., Rubiolo, J. A., Gómez-Garrido, J., Carreté, L., Bello, X., Gut, M., Gut, I. G., Marcet-Houben, M., Forn-Cuní, G., Galán, B., García, J. L., Abal-Fabeiro, J. L., Pardo, B. G., Taboada, X., Fernández, C., … Martínez, P. (2016). Whole genome sequencing of turbot (Scophthalmus maximus; Pleuronectiformes): A fish adapted to demersal life. DNA Research, 23, 181-192. https://doi.org/10.1093/dnares/dsw007
Gao, B., Shen, D., Xue, S., Chen, C., Cui, H., & Song, C. (2016). The contribution of transposable elements to size variations between four teleost genomes. Mobile DNA, 7, 4. https://doi.org/10.1186/s13100-016-0059-7
García-Cegarra, A., Merlo, M. A., Ponce, M., Portela-Bens, S., Cross, I., Manchado, M., & Rebordinos, L. (2013). A preliminary genetic map in Solea senegalensis (pleuronectiformes, soleidae) using BAC-FISH and next-generation sequencing. Cytogenetic and Genome Research, 14, 227-240. https://doi.org/10.1159/000355001
Guerrero-Cózar, I., Gomez-Garrido, J., Berbel, C., Martinez-Blanch, J. F., Alioto, T., Claros, M. G., Gagnaire, P. A., & Manchado, M. (2021). Chromosome anchoring in Senegalese sole (Solea senegalensis) reveals sex-associated markers and genome rearrangements in flatfish. Scientific Reports, 11, 13460. https://doi.org/10.1038/s41598-021-92601-5
Guiguen, Y., Fostier, A., & Herpin, A. (2019). Sex determination and differentiation in fish: Genetic, genomic, and endocrine aspects. In H.-P. Wang, F. Piferrer, S.-L. Chen, & Z.-G. Shen (Eds.), Sex control in aquaculture (Vol. 1, pp. 35-63). John Wiley & Sons Ltd.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321. https://doi.org/10.1093/sysbio/syq010
Haas, B. J., Salzberg, S. L., Zhu, W., Pertea, M., Allen, J. E., Orvis, J., White, O., Buell, C. R., & Wortman, J. R. (2008). Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biololgy, 9, R7. https://doi.org/10.1186/gb-2008-9-1-r7
Hao, Z., Lv, D., Ge, Y., Shi, J., Weijers, D., Yu, G., & Chen, J. (2020). RIdeogram: Drawing SVG graphics to visualize and map genome-wide data on the idiograms. PeerJ Computer Science, 6, e251. https://doi.org/10.7717/peerj-cs.251
Hattori, R. S., Murai, Y., Oura, M., Masuda, S., Majhi, S. K., Sakamoto, T., Fernandino, J. I., Somoza, G. M., Yokota, M., & Strus̈smann, C. A. (2012). A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proceedings of the National Academy of Sciences USA, 109, 2955-2959. https://doi.org/10.1073/pnas.1018392109
Hayashi, Y., Kobira, H., Yamaguchi, T., Shiraishi, E., Yazawa, T., Hirai, T., Kamei, Y., & Kitano, T. (2010). High temperature causes masculinization of genetically female medaka by elevation of cortisol. Molecular Reproduction and Development, 77, 679-686. https://doi.org/10.1002/mrd.21203
Herpin, A., Schartl, M., Depincé, A., Guiguen, Y., Bobe, J., Hua-Van, A., Hayman, E. S., Octavera, A., Yoshizaki, G., Nichols, K. M., Goetz, G. W., & Luckenbach, J. A. (2021). Allelic diversification after transposable element exaptation promoted gsdf as the master sex determining gene of sablefish. Genome Research, 31, 1366-1381. https://doi.org/10.1101/gr.274266.120
Hu, J., Fan, J., Sun, Z., & Liu, S. (2020). NextPolish: A fast and efficient genome polishing tool for long-read assembly. Bioinformatics, 36, 2253-2255. https://doi.org/10.1093/bioinformatics/btz891
Huerta-Cepas, J., Serra, F., & Bork, P. (2016). ETE 3: Reconstruction, analysis, and visualization of Phylogenomic data. Molecular Biology and Evolution, 33, 1635-1638. https://doi.org/10.1093/molbev/msw046
Ishida, T., & Kinoshita, K. (2007). PrDOS: Prediction of disordered protein regions from amino acid sequence. Nucleic Acids Research, 35, W460-W464. https://doi.org/10.1093/nar/gkm363
Jasonowicz, A. J., Simeon, A. E., Zahm, M., Cabau, C., Klopp, C., Roques, C., Lampietro, C., Lluch, J., Donnadieu, C., Parrinello, H., Drinan, D., Hauser, L., Guiguen, Y., & Planas, J. V. (2022). Generation of a chromosome-level genome assembly for Pacific halibut (Hippoglossus stenolepis) and characterization of its sex-determining region. Molecular Ecology Resources, 22, 2685-2700. https://doi.org/10.1111/1755-0998.13641
Jones, D. T., & Cozzetto, D. (2015). DISOPRED3: Precise disordered region predictions with annotated protein-binding activity. Bioinformatics, 31, 857-863. https://doi.org/10.1093/bioinformatics/btu744
Jones, P., Binns, D., Chang, H. Y., Fraser, M., Li, W., McAnulla, C., McWilliam, H., Maslen, J., Mitchell, A., Nuka, G., Pesseat, S., Quinn, A. F., Sangrador-Vegas, A., Scheremetjew, M., Yong, S. Y., López, R., & Hunter, S. (2014). InterProScan 5: Genome-scale protein function classification. Bioinformatics, 30, 1236-1240. https://doi.org/10.1093/bioinformatics/btu031
Kamiya, T., Kai, W., Tasumi, S., Oka, A., Matsunaga, T., Mizuno, N., Fujita, M., Suetake, H., Suzuki, S., Hosoya, S., Tohari, S., Brenner, S., Miyadai, T., Venkatesh, B., Suzuki, Y., & Kikuchi, K. (2012). A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (Fugu). PLoS Genetics, 8, e1002798. https://doi.org/10.1371/journal.pgen.1002798
Kobayashi, Y., Nozu, R., & Nakamura, M. (2017). Expression and localization of two gonadotropin receptors in gonads of the yellowtail clownfish, Amphiprion clarkii. Journal of Aquaculture & Marine Biology, 5, 120. https://doi.org/10.15406/jamb.2017.05.00120
Koyama, T., Nakamoto, M., Morishima, K., Yamashita, R., Yamashita, T., Sasaki, K., Kuruma, Y., Mizuno, N., Suzuki, M., Okada, Y., Ieda, R., Uchino, T., Tasumi, S., Hosoya, S., Uno, S., Koyama, J., Toyoda, A., Kikuchi, K., & Sakamoto, T. (2019). A SNP in a steroidogenic enzyme is associated with phenotypic sex in Seriola fishes. Current Biology, 29, 1901-1909.e8. https://doi.org/10.1016/j.cub.2019.04.069
Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J., & Marra, M. A. (2009). Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639-1645. https://doi.org/10.1101/gr.092759.109
Kubista, M., Sindelka, R., Tichopad, A., Bergkvist, A., Lindh, D., & Forootan, A. (2007). The prime technique. Real-time PCR data analysis. GIT Laboratory Journal, 9-10, 33-35.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25. https://doi.org/10.1186/gb-2009-10-3-r25
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948. https://doi.org/10.1093/bioinformatics/btm404
Levavi-Sivan, B., Bogerd, J., Mañanós, E. L., Gómez, A., & Lareyre, J. J. (2010). Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology, 165, 412-437. https://doi.org/10.1016/j.ygcen.2009.07.019
Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27, 2987-2993. https://doi.org/10.1093/bioinformatics/btr509
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics, 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
Lomsadze, A., Burns, P. D., & Borodovsky, M. (2014). Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Research, 42, e119. https://doi.org/10.1093/nar/gku557
Lü, Z., Gong, L., Ren, Y., Chen, Y., Wang, Z., Liu, L., Li, H., Chen, X., Li, Z., Luo, H., Jiang, H., Zeng, Y., Wang, Y., Wang, K., Zhang, C., Jiang, H., Wan, W., Qin, Y., Zhang, J., … Li, Y. (2021). Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan. Nature Genetics, 53, 742-751. https://doi.org/10.1038/s41588-021-00836-9
Luckenbach, J. A., Borski, R. J., Daniels, H. V., & Godwin, J. (2009). Sex determination in flatfishes: Mechanisms and environmental influences. Seminars in Cell & Developmental Biology, 20, 256-263. https://doi.org/10.1016/j.semcdb.2008.12.002
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. (2018). 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. DNA Research, 25, 439-450. https://doi.org/10.1093/dnares/dsy015
Martín, I., Carazo, I., Rasines, I., Rodríguez, C., Fernández, R., Martínez, P., Norambuena, F., Chereguini, O., & Duncan, N. (2019). Reproductive performance of captive Senegalese sole, Solea senegalensis, according to the origin (wild or cultured) and gender. Spanish Journal of Agricultural Research, 17, e0608. https://doi.org/10.5424/sjar/2019174-14953
Martínez, P., Robledo, D., Taboada, X., Blanco, A., Moser, M., Maroso, F., Hermida, M., Gómez-Tato, A., Álvarez-Blázquez, B., Cabaleiro, S., Piferrer, F., Bouza, C., Lien, S., & Viñas, A. M. (2021). A genome-wide association study, supported by a new chromosome-level genome assembly, suggests sox2 as a main driver of the undifferentiated ZZ/ZW sex determination of turbot (Scophthalmus maximus). Genomics, 113, 1705-1718.
Martínez, P., Viñas, A. M., Sánchez, L., Díaz, N., Ribas, L., & Piferrer, F. (2014). Genetic architecture of sex determination in fish: Applications to sex ratio control in aquaculture. Frontiers in Genetics, 5, 340. https://doi.org/10.3389/fgene.2014.00340
Matsuda, M., Nagahama, Y., Shinomiya, A., Sato, T., Matsuda, C., Kobayashi, T., Morrey, C. E., Shibata, N., Asakawa, S., Shimizu, N., Hori, H., Hamaguchi, S., & Sakaizumi, M. (2002). DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature, 417, 559-563. https://doi.org/10.1038/nature751
Molina-Luzón, M. J., López, J. R., Robles, F., Navajas-Pérez, R., Ruiz-Rejón, C., De la Herrán, R., & Navas, J. I. (2015). Chromosomal manipulation in Senegalese sole (Solea senegalensis Kaup, 1858): Induction of triploidy and gynogenesis. Journal of Applied Genetics, 56, 77-84. https://doi.org/10.1007/s13353-014-0233-x
Morais, S., Aragão, C., Cabrita, E., Conceição, L. E., Constenla, M., Costas, B., … Dinis, M. T. (2016). New developments and biological insights into the farming of Solea senegalensis reinforcing its aquaculture potential. Reviews in Aquaculture, 8(3), 227-263. https://doi.org/10.1111/raq.12091
Murozumi, N., Nakashima, R., Hirai, T., Kamei, Y., Ishikawa-Fujiwara, T., Todo, T., & Kitano, T. (2014). Loss of follicle-stimulating hormone receptor function causes masculinization and suppression of ovarian development in genetically female medaka. Endocrinology, 155, 3136-3145. https://doi.org/10.1210/en.2013-2060
Myosho, T., Otake, H., Masuyama, H., Matsuda, M., Kuroki, Y., Fujiyama, A., Naruse, K., Hamaguchi, S., & Sakaizumi, M. (2012). Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics, 191, 163-170. https://doi.org/10.1534/genetics.111.137497
Nacif, C. L., Kratochwil, C. F., Kautt, A. F., Nater, A., Machado-Schiaffino, G., Meyer, A., & Henning, F. (2022). Molecular parallelism in the evolution of a master sex-determining role for the anti-Mullerian hormone receptor 2 gene (amhr2) in Midas cichlids. Molecular Ecology, 1-13. http://doi.org/10.1111/mec.16466
Nakamoto, M., Uchino, T., Koshimizu, E., Kuchiishi, Y., Sekiguchi, R., Wang, L., Sudo, R., Endo, M., Guiguen, Y., Schartl, M., Postlethwait, J. H., & Sakamoto, T. (2021). A Y-linked anti-Müllerian hormone type-II receptor is the sex-determining gene in ayu, Plecoglossus altivelis. PLoS Genetics, 17, e1009705. https://doi.org/10.1371/journal.pgen.1009705
Nawrocki, E. P., Burge, S. W., Bateman, A., Daub, J., Eberhardt, R. Y., Eddy, S. R., Floden, E. W., Gardner, P. P., Jones, T. A., Tate, J., & Finn, R. D. (2015). Rfam 12.0: Updates to the RNA families database. Nucleic Acids Research, 43, D130-D137. https://doi.org/10.1093/nar/gku1063
Nawrocki, E. P., & Eddy, S. R. (2013). Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics, 29, 2933-2935. https://doi.org/10.1093/bioinformatics/btt509
Pan, Q., Feron, R., Yano, A., Guyomard, R., Jouanno, E., Vigouroux, E., Wen, M., Busne, J. M., Bobe, J., Concordet, J. P., et al. (2019). Identification of the master sex determining gene in northern pike (Esox lucius) reveals restricted sex chromosome differentiation. PLoS Genetics, 15, e1008013. https://doi.org/10.1371/journal.pgen.1008013
Parra, G., Blanco, E., & Guigo, R. (2000). GeneID in drosophila. Genome Research, 10, 511-515. https://doi.org/10.1101/gr.10.4.511
Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T. C., Mendell, J. T., & Salzberg, S. L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-Seq reads. Nature Biotechnology, 33, 290-295. https://doi.org/10.1038/nbt.3122
Ramírez, D., Rodríguez, M. E., Cross, I., Arias-Pérez, A., Merlo, M. A., Anaya, M., Portela-Bens, S., Martínez, P., Robles, F., Ruiz-Rejón, C., & Rebordinos, L. (2022). Integration of maps enables a Cytogenomics analysis of the complete karyotype in Solea senegalensis. International Journal of Molecular Sciences, 23, 5353. https://doi.org/10.3390/ijms23105353
Ramos, L., & Antunes, A. (2022). Decoding sex: Elucidating sex determination and how high-quality genome assemblies are untangling the evolutionary dynamics of sex chromosomes. Genomics, 114, 110277. https://doi.org/10.1016/j.ygeno.2022.110277
Ramos-Júdez, S., González-López, W. Á., Ostos, J. H., Mamani, N. C., Alemán, C. M., Beirão, J., & Duncan, N. (2021). Low sperm to egg ratio required for successful in vitro fertilization in a pair-spawning teleost, Senegalese sole (Solea senegalensis). Royal Society Open Science, 8, 201718. https://doi.org/10.1098/rsos.201718
Raymond, M., & Rousset, F. (1995). GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Rhie, A., Walenz, B. P., Koren, S., & Phillippy, A. M. (2020). Merqury: Reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biology, 21, 245. https://doi.org/10.1186/s13059-020-02134-9
Robinson, J. T., Thorvaldsdóttir, H., Wenger, A. M., Zehir, A., & Merisov, J. P. (2017). Variant review with the integrative genomics viewer (IGV). Cancer Research, 77, 31-34. https://doi.org/10.1158/0008-5472.CAN-17-0337
Robledo, D., Fernández, C., Hermida, M., Sciara, A., Álvarez-Dios, J. A., Cabaleiro, S., Caamaño, R., Martínez, P., & Bouza, C. (2016). Integrative transcriptome, genome and quantitative trait loci resources identify single nucleotide polymorphisms in candidate genes for growth traits in turbot. International Journal of Molecular Sciences, 17(2), 243. https://doi.org/10.3390/ijms17020243
Robledo, D., Hermida, M., Rubiolo, J. A., Fernández, C., Blanco, A., Bouza, C., & Martínez, P. (2017). Integrating genomic resources of flatfish (Pleuronectiformes) to boost aquaculture production. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 21, 41-55. https://doi.org/10.1016/j.cbd.2016.12.001
Robledo, D., Hernández-Urcera, J., Cal, R. M., Pardo, B. G., Sánchez, L., Martínez, P., & Viñas, A. (2014). Analysis of qPCR reference gene stability determination methods and a practical approach for efficiency calculation on a turbot (Scophthalmus maximus) gonad dataset. BMC Genomics, 15, 648. https://doi.org/10.1186/1471-2164-15-648
Robledo, D., Ribas, L., Cal, R., Sánchez, L., Piferrer, F., Martínez, P., & Viñas, A. (2015). Gene expression analysis at the onset of sex differentiation in turbot (Scophthalmus maximus). BMC Genomics, 16, 973. https://doi.org/10.1186/s12864-015-2142-8
Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., & Dunker, A. K. (2001). Sequence complexity of disordered protein. Proteins, 42, 38-48. https://doi.org/10.1002/1097-0134(20010101)42:1<38::aid-prot50>3.0.co;2-3
Rozen, S., & Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology, 132, 365-386. https://doi.org/10.1385/1-59259-192-2:365
Sambroni, E., Lareyre, J. J., & le Gac, F. (2013). Fsh controls gene expression in fish both independently of and through steroid mediation. PLoS One, 8, e76684. https://doi.org/10.1371/journal.pone.0076684
Shao, C., Bao, B., Xie, Z., Chen, X., Li, B., Jia, X., Yao, Q., Ortí, G., Li, W., Li, X., Hamre, K., Xu, J., Wang, L., Chen, F., Tian, Y., Schreiber, A. M., Wang, N., Wei, F., Zhang, J., … Chen, S. (2017). The genome and transcriptome of Japanese flounder provide insights into flatfish asymmetry. Nature Genetics, 49, 119-124. https://doi.org/10.1038/ng.3732
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212. https://doi.org/10.1093/bioinformatics/btv351
Slater, G. S., & Birney, E. (2005). Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics, 6, 31. https://doi.org/10.1186/1471-2105-6-31
Stam, P. (1993). Construction of integrated genetic linkage maps by means of a new computer package: JOINMAP. The Plant Journal, 3, 739-744. https://doi.org/10.1111/j.1365-313X.1993.00739.x
Stanke, M., Schoffmann, O., Morgenstern, B., & Waack, S. (2006). Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics, 7, 62. https://doi.org/10.1186/1471-2105-7-62
Taboada, X., Pansonato-Alves, J. C., Foresti, F., Martínez, P., Viñas, A., Pardo, B. G., & Bouza, C. (2014). Consolidation of the genetic and cytogenetic maps of turbot (Scophthalmus maximus) using FISH with BAC clones. Chromosoma, 123, 281-291. https://doi.org/10.1007/s00412-014-0452-2
Takehana, Y., Matsuda, M., Myosho, T., Suster, M. L., Kawakami, K., Shin-I, T., Kohara, Y., Kuroki, Y., Toyoda, A., Fujiyama, A., Hamaguchi, S., Sakaizumi, M., & Naruse, K. (2014). Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nature Communications, 5, 4157. https://doi.org/10.1038/ncomms5157
Ulloa-Aguirre, A., Zariñán, T., Jardón-Valadez, E., Gutiérrez-Sagal, R., & Dias, J. A. (2018). Structure-function relationships of the follicle-stimulating hormone receptor. Frontiers in Endocrinology (Lausanne), 9, 707. https://doi.org/10.3389/fendo.2018.00707
Vega, L., Díaz, E., Cross, I., & Rebordinos, L. (2002). Caracterizaciones citogenética e isoenzimática del lenguado Solea senegalensis Kaup, 1858. Boletín. Instituto Español de Oceanografía, 18, 245-250.
Viñas, J., Asensio, E., Cañavate, J. P., & Piferrer, F. (2013). Gonadal sex differentiation in the Senegalese sole (Solea senegalensis) and first data on the experimental manipulation of its sex ratios. Aquaculture, 384-387, 74-81. https://doi.org/10.1016/j.aquaculture.2012.12.012
Voorrips, R. E. (2002). Mapchart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93, 77-78. https://doi.org/10.1093/jhered/93.1.77
Wang, L., Sun, F., Wan, Z. Y., Yang, Z., Tay, Y. X., Lee, M., Ye, B., Wen, Y., Meng, Z., Fan, B., Alfiko, Y., Shen, Y., Piferrer, F., Meyer, A., Schartl, M., & Yue, G. H. (2022). Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish. BMC Biology, 20, 5. https://doi.org/10.1186/s12915-021-01205-y
Wang, S., Meyer, E., Mckay, J. K., & Matz, M. V. (2012). 2b-RAD: A simple and flexible method for genome-wide genotyping. Nature Methods, 9, 808-810. https://doi.org/10.1038/nmeth.2023
Wen, M., Pan, Q., Jouanno, E., Montfort, J., Zahm, M., Cabau, C., Klopp, C., Iampietro, C., Roques, C., Bouchez, O., Castinel, A., Donnadieu, C., Parrinello, H., Poncet, C., Belmonte, E., Gautier, V., Avarre, J. C., Dugue, R., Gustiano, R., … Guiguen, Y. (2022). An ancient truncated duplication of the anti-Mullerian hormone receptor type 2 geneis apotential conserved master sex determinant in the Pangasiidae catfish family. Molecular Ecology Resources, 22, 2411-2428. https://doi.org/10.1111/1755-0998.13620
Wu, Y., Close, T. J., & Lonardi, S. (2011). Accurate construction of consensus genetic maps via integer linear programming. IEEE/ACM Transactions on Computational Biology and Bioinformatics, 8, 381-394. https://doi.org/10.1109/TCBB.2010.35
Yano, A., Nicol, B., Jouanno, E., Quillet, E., Fostier, A., Guyomard, R., & Guiguen, Y. (2013). The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evolutionary Applications, 6, 486-496. https://doi.org/10.1111/eva.12032
Zariñán, T., Perez-Solís, M. A., Maya-Núñez, G., Casas-González, P., Conn, P. M., Dias, J. A., & Ulloa-Aguirre, A. (2010). Dominant negative effects of human follicle-stimulating hormone receptor expression-deficient mutants on wild-type receptor cell surface expression. Rescue of oligomerization-dependent defective receptor expression by using cognate decoys. Molecular and Cellular Endocrinology, 321, 112-122. https://doi.org/10.1016/j.mce.2010.02.027
Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Informatics, 9, 40. https://doi.org/10.1186/1471-2105-9-40
Zhang, Z., Lau, S. W., Zhang, L., & Ge, W. (2015). Disruption of zebrafish follicle-stimulating hormone receptor (fshr) but not luteinizing hormone receptor (lhcgr) gene by TALEN leads to failed follicle activation in females followed by sexual reversal to males. Endocrinology (United States), 156, 3747-3762. https://doi.org/10.1210/en.2015-1039
Zheng, S., Tao, W., Yang, H., Kocher, T. D., Wang, Z., Peng, Z., Jin, L., Pu, D., Zhang, Y., & Wang, D. (2022). Identification of sex chromosome and sex-determining gene of southern catfish (Silurus meridionalis) based on XX, XY and YY genome sequencing. Proceedings of the Royal Society B, 289, 20212645. https://doi.org/10.1098/rspb.2021.2645