Mechanisms of sex differentiation and sex reversal in hermaphrodite fish as revealed by the Epinephelus coioides genome.

Epinephelus coioides chromosome-level genome assembly sex differentiation sex reversal socially controlled sex change transcriptomics

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
Historique:
revised: 13 12 2022
received: 26 02 2022
accepted: 28 12 2022
medline: 6 4 2023
pubmed: 12 1 2023
entrez: 11 1 2023
Statut: ppublish

Résumé

Most grouper species are functional protogynous hermaphrodites, but the genetic basis and the molecular mechanisms underlying the regulation of this unique reproductive strategy remain enigmatic. In this study, we report a high-quality chromosome-level genome assembly of the representative orange-spotted grouper (Epinephelus coioides). No duplication or deletion of sex differentiation-related genes was found in the genome, suggesting that sex development in this grouper may be related to changes in regulatory sequences or environmental factors. Transcriptomic analyses showed that aromatase and retinoic acid are probably critical to promoting ovarian fate determination, and follicle-stimulating hormone triggers the female-to-male sex change. Socially controlled sex-change studies revealed that, in sex-changing fish, the brain's response to the social environment may be mediated by activation of the phototransduction cascade and the melatonin synthesis pathway. In summary, our genomic and experimental results provide novel insights into the molecular mechanisms of sex differentiation and sex change in the protogynous groupers.

Identifiants

pubmed: 36631404
doi: 10.1111/1755-0998.13753
doi:

Substances chimiques

Fish Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

920-932

Subventions

Organisme : Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams
ID : 2019KJ143
Organisme : Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai)
ID : 311021006
Organisme : Key-Area Research and Development Program of Guangdong Province
ID : 2021B0202020002
Organisme : National Natural Science Foundation of China
ID : 31972769
Organisme : National Natural Science Foundation of China
ID : 31902346
Organisme : National Natural Science Foundation of China
ID : 32172968
Organisme : Natural Science Foundation for Fundamental Research in Shenzhen
ID : JCYJ20190812105801661

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Avise, J., & Mank, J. (2009). Evolutionary perspectives on hermaphroditism in fishes. Sexual Development, 3(2-3), 152-163.
Bao, W., Kojima, K. K., & Kohany, O. (2015). Repbase update, a database of repetitive elements in eukaryotic genomes. Mobile DNA, 6(1), 1-6.
Benson, G. (1999). Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research, 27(2), 573-580.
Bertho, S., Herpin, A., Branthonne, A., Jouanno, E., Yano, A., Nicol, B., Muller, T., Pannetier, M., Pailhoux, E., Miwa, M., Yoshizaki, G., Schartl, M., & Guiguen, Y. (2018). The unusual rainbow trout sex determination gene hijacked the canonical vertebrate gonadal differentiation pathway. Proceedings of the National Academy of Sciences, 115(50), 12781-12786.
Bertho, S., Herpin, A., Schartl, M., & Guiguen, Y. (2021). Lessons from an unusual vertebrate sex-determining gene. Philosophical Transactions of the Royal Society B, 376(1832), 20200092.
Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J., Hamada, H., & Koopman, P. (2006). Retinoid signaling determines germ cell fate in mice. Science, 312(5773), 596-600.
Cantarel, B. L., Korf, I., Robb, S. M., Parra, G., Ross, E., Moore, B., Holt, C., Sánchez Alvarado, A., & Yandell, M. (2008). MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Research, 18(1), 188-196.
Cardoso, S. D., Teles, M. C., & Oliveira, R. F. (2015). Neurogenomic mechanisms of social plasticity. Journal of Experimental Biology, 218(1), 140-149.
Casas, L., Saborido-Rey, F., Ryu, T., Michell, C., Ravasi, T., & Irigoien, X. (2016). Sex change in clownfish: Molecular insights from transcriptome analysis. Scientific Reports, 6(1), 1-19.
Chaisson, M. J., & Tesler, G. (2012). Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): Application and theory. BMC Bioinformatics, 13(1), 1-18.
Chen, J., Peng, C., Huang, J., Shi, H., Xiao, L., Tang, L., Lin, H., Li, S., & Zhang, Y. (2021). Physical interactions facilitate sex change in the protogynous orange-spotted grouper, Epinephelus coioides. Journal of Fish Biology, 98(5), 1308-1320.
Coccaro, E. F., Lee, R., & Coussons-Read, M. (2015). Cerebrospinal fluid inflammatory cytokines and aggression in personality disordered subjects. International Journal of Neuropsychopharmacology, 18(7), pyv001.
Cui, Z., Liu, Y., Wang, W., Wang, Q., Zhang, N., Lin, F., Wang, N., Shao, C., Dong, Z., Li, Y., Yang, Y., Hu, M., Li, H., Gao, F., Wei, Z., Meng, L., Liu, Y., Wei, M., Zhu, Y., … Chen, S. (2017). Genome editing reveals dmrt1 as an essential male sex-determining gene in Chinese tongue sole (Cynoglossus semilaevis). Scientific reports, 7(1), 1-10.
De Bie, T., Cristianini, N., Demuth, J. P., & Hahn, M. W. (2006). CAFE: A computational tool for the study of gene family evolution. Bioinformatics, 22(10), 1269-1271.
De Mitcheson, Y. S., & Liu, M. (2008). Functional hermaphroditism in teleosts. Fish and Fisheries, 9(1), 1-43.
Deveson, I. W., Holleley, C. E., Blackburn, J., Marshall Graves, J. A., Mattick, J. S., Waters, P. D., & Georges, A. (2017). Differential intron retention in Jumonji chromatin modifier genes is implicated in reptile temperature-dependent sex determination. Science Advances, 3(6), e1700731.
Erisman, B. E., Petersen, C. W., Hastings, P. A., & Warner, R. R. (2013). Phylogenetic perspectives on the evolution of functional hermaphroditism in teleost fishes. Integrative and Comparative Biology, 53(4), 736-754.
Falcón, J. (1999). Cellular circadian clocks in the pineal. Progress in Neurobiology, 58(2), 121-162.
Garcia, C. E., Araújo, B. C., Mello, P. H., Narcizo, A. D. M., Rodrigues-Filho, J. A., Medrado, A. T., Zampieri, R. A., Floeter-Winter, L. M., & Moreira, R. G. (2013). Involvement of pituitary gonadotropins, gonadal steroids and breeding season in sex change of protogynous dusky grouper, Epinephelus marginatus (Teleostei: Serranidae), induced by a non-steroidal aromatase inhibitor. General and Comparative Endocrinology, 192, 170-180.
Godwin, J. (2009). Social determination of sex in reef fishes. Paper presented at the seminars in cell & developmental biology. Academic Press, 20(3), 264-270.
Godwin, J., Crews, D., & Warner, R. R. (1996). Behavioural sex change in the absence of gonads in a coral reef fish. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263(1377), 1683-1688.
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., … Regev, A. (2011). Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnology, 29(7), 644.
Guiguen, Y., Fostier, A., Piferrer, F., & Chang, C.-F. (2010). Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. General and Comparative Endocrinology, 165(3), 352-366.
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(3), 307-321.
Hattori, R. S., Murai, Y., Oura, M., Masuda, S., Majhi, S. K., Sakamoto, T., Fernandino, J. I., Somoza, G. M., Yokota, M., & Strüssmann, C. (2012). A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proceedings of the National Academy of Sciences, 109(8), 2955-2959.
He, Z., Deng, F., Yang, D., He, Z., Hu, J., Ma, Z., Zhang, Q., He, J., Ye, L., Chen, H., & He, L. (2022). Crosstalk between sex-related genes and apoptosis signaling reveals molecular insights into sex change in a protogynous hermaphroditic teleost fish, ricefield eel Monopterus albus. Aquaculture, 552, 737918.
Heemstra, P. C., & Randall, J. E. (1993). Groupers of the world. FAO Fisheries Synopsis, 16(125), I.
Huang, M., Wang, Q., Chen, J., Chen, H., Xiao, L., Zhao, M., Zhang, H., Li, S., Liu, Y., Zhang, Y., & Lin, H. (2019). The co-administration of estradiol/17α-methyltestosterone leads to male fate in the protogynous orange-spotted grouper, Epinephelus coioides. Biology of Reproduction, 100(3), 745-756.
Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., & Walichiewicz, J. (2005). Repbase update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research, 110(1-4), 462-467.
Kajitani, R., Toshimoto, K., Noguchi, H., Toyoda, A., Ogura, Y., Okuno, M., Yabana, M., Harada, M., Nagayasu, E., Maruyama, H., Kohara, Y., Fujiyama, A., Hayashi, T., & Itoh, T. (2014). Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Research, 24(8), 1384-1395.
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(7), e1002798.
Kline, R. J., Khan, I. A., & Holt, G. J. (2011). Behavior, color change and time for sexual inversion in the protogynous grouper (Epinephelus adscensionis). PLoS One, 6(5), e19576.
Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P., & Lovell-Badge, R. (1991). Male development of chromosomally female mice transgenic for Sry. Nature, 351(6322), 117-121.
Lamm, M. S., Liu, H., Gemmell, N. J., & Godwin, J. R. (2015). The need for speed: Neuroendocrine regulation of socially-controlled sex change. Integrative and Comparative Biology, 55(2), 307-322.
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357-359.
Li, B., & Dewey, C. N. (2011). RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1), 1-16.
Li, F., Li, Z., Wang, Q., & Zhai, Y. (2013). Effects of BPA and E2 on expression profiles of genes related to hypothalamic-pituitary-gonadal axis of half-smooth tongue sole Cynoglossus semilaevis. Chinese Journal of Oceanology and Limnology, 31(3), 598-608.
Li, H., Coghlan, A., Ruan, J., Coin, L. J., Heriche, J.-K., Osmotherly, L., Li, R., Liu, T., Zhang, Z., Bolund, L., Wong, G. K., Zheng, W., Dehal, P., Wang, J., & Durbin, R. (2006). TreeFam: A curated database of phylogenetic trees of animal gene families. Nucleic Acids Research, 34(suppl_1), D572-D580.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760.
Liu, M., & de Mitcheson, Y. S. (2009). Gonad development during sexual differentiation in hatchery-produced orange-spotted grouper (Epinephelus coioides) and humpback grouper (Cromileptes altivelis) (Pisces: Serranidae, Epinephelinae). Aquaculture, 287(1-2), 191-202.
Luiz, O. J., Woods, R. M., Madin, E. M., & Madin, J. S. (2016). Predicting IUCN extinction risk categories for the world's data deficient groupers (Teleostei: Epinephelidae). Conservation Letters, 9(5), 342-350.
Mackie, M. (2003). Socially controlled sex-change in the half-moon grouper, Epinephelus rivulatus, at Ningaloo Reef, Western Australia. Coral Reefs, 22(2), 133-142.
Mank, J. E., Promislow, D. E., & Avise, J. C. (2006). Evolution of alternative sex-determining mechanisms in teleost fishes. Biological Journal of the Linnean Society, 87(1), 83-93.
Morris, A. V., Roberts, C. M., & Hawkins, J. P. (2000). The threatened status of groupers (Epinephelinae). Biodiversity & Conservation, 9(7), 919-942.
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(1), 163-170.
Pamilo, P., & O'Neill, R. (1997). Evolution of the Sry genes. Molecular Biology and Evolution, 14(1), 49-55.
Pauletto, M., Manousaki, T., Ferraresso, S., Babbucci, M., Tsakogiannis, A., Louro, B., Vitulo, N., Quoc, V. H., Carraro, R., Bertotto, D., Franch, R., Maroso, F., Aslam, M. L., Sonesson, A. K., Simionati, B., Malacrida, G., Cestaro, A., Caberlotto, S., Sarropoulou, E., … Bargelloni, L. (2018). Genomic analysis of Sparus aurata reveals the evolutionary dynamics of sex-biased genes in a sequential hermaphrodite fish. Communications Biology, 1(1), 1-13.
Sadovy de Mitcheson, Y., Craig, M. T., Bertoncini, A. A., Carpenter, K. E., Cheung, W. W., Choat, J. H., Cornish, A. S., Fennessy, S. T., Ferreira, B. P., Heemstra, P. C., & Liu, M. (2013). Fishing groupers towards extinction: A global assessment of threats and extinction risks in a billion dollar fishery. Fish and Fisheries, 14(2), 119-136.
Senthilkumaran, B., Yoshikuni, M., & Nagahama, Y. (2004). A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Molecular and Cellular Endocrinology, 215(1-2), 11-18.
Shapiro, D. Y., Garcia-Moliner, G., & Sadovy, Y. (1994). Social system of an inshore stock of the red hind grouper, Epinephelus guttatus (Pisces: Serranidae). In Women in ichthyology: An anthology in honour of ET, Ro and Genie (pp. 415-422). Springer.
Shen, Z. G., & Wang, H. P. (2018). Environmental sex determination and sex differentiation in teleosts-how sex is established. Sex Control in Aquaculture, 85-115.
Shi, Q. (2005). Melatonin is involved in sex change of the ricefield eel, Monopterus albus Zuiew. Reviews in Fish Biology and Fisheries, 15(1), 23-36.
Sinclair, A. H., Berta, P., Palmer, M. S., Hawkins, J. R., Griffiths, B. L., Smith, M. J., Foster, J. W., Frischauf, A. M., Lovell-Badge, R., & Goodfellow, P. N. (1990). A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature, 346(6281), 240-244.
Stanke, M., & Waack, S. (2003). Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics, 19(suppl_2), ii215-ii225.
Takahashi, A., Flanigan, M. E., McEwen, B. S., & Russo, S. J. (2018). Aggression, social stress, and the immune system in humans and animal models. Frontiers in Behavioral Neuroscience, 12, 56.
Tarailo-Graovac, M., & Chen, N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Current proTOCOLS IN BIOINFORMATICS, 25(1), 4.10. 11-14.10. 14.
Tian, H.-F., Hu, Q.-M., & Li, Z. (2021). A high-quality de novo genome assembly of one swamp eel (Monopterus albus) strain with PacBio and Hi-C sequencing data. G3, 11(1), jkaa032.
Todd, E. V., Ortega-Recalde, O., Liu, H., Lamm, M. S., Rutherford, K. M., Cross, H., Black, M. A., Kardailsky, O., Marshall Graves, J. A., Hore, T. A., Godwin, J. R., & Gemmell, N. J. (2019). Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Science Advances, 5(7), eaaw7006.
Van der Auwera, G. A., Carneiro, M. O., Hartl, C., Poplin, R., Del Angel, G., Levy-Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., Banks, E., Garimella, K. V., Altshuler, D., Gabriel, S., & DePristo, M. A. (2013). From FastQ data to high-confidence variant calls: The genome analysis toolkit best practices pipeline. Current Protocols in Bioinformatics, 43(1), 11.10. 11-11.10. 33.
Wang, D., Zhang, J., & Zhang, Z. (2012). Effect of testosterone and melatonin on social dominance and agonistic behavior in male Tscheskia triton. Behavioural Processes, 89(3), 271-277.
Warner, R. R., & Swearer, S. E. (1991). Social control of sex change in the bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). The Biological Bulletin, 181(2), 199-204.
Wu, G.-C., Tey, W.-G., Li, H.-W., & Chang, C.-F. (2015). Sexual fate reprogramming in the steroid-induced bi-directional sex change in the protogynous orange-spotted grouper, Epinephelus coioides. PLoS One, 10(12), e0145438.
Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C. Y., & Wei, L. (2011). KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research, 39(suppl_2), W316-W322.
Xu, Z., & Wang, H. (2007). LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research, 35(suppl_2), W265-W268.
Ye, C., Hill, C. M., Wu, S., Ruan, J., & Ma, Z. S. (2016). DBG2OLC: Efficient assembly of large genomes using long erroneous reads of the third generation sequencing technologies. Scientific Reports, 6(1), 1-9.
You, X., Shu, L., Li, S., Chen, J., Luo, J., Lu, J., Mu, Q., Bai, J., Xia, Q., Chen, Q., Cai, Y., Zhang, H., Chen, G., Lin, H., Zhang, Y., & Shi, Q. (2013). Construction of high-density genetic linkage maps for orange-spotted grouper Epinephelus coioides using multiplexed shotgun genotyping. BMC Genetics, 14(1), 1-8.
Zalcman, S. S., & Siegel, A. (2006). The neurobiology of aggression and rage: Role of cytokines. Brain, Behavior, and Immunity, 20(6), 507-514.
Zhang, W., Lu, H., Jiang, H., Li, M., Zhang, S., Liu, Q., & Zhang, L. (2012). Isolation and characterization of cyp19a1a and cyp19a1b promoters in the protogynous hermaphrodite orange-spotted grouper (Epinephelus coioides). General and Comparative Endocrinology, 175(3), 473-487.
Zhang, Z., Zhang, K., Chen, S., Zhang, Z., Zhang, J., You, X., Bian, C., Xu, J., Jia, C., Qiang, J., Zhu, F., Li, H., Liu, H., Shen, D., Ren, Z., Chen, J., Li, J., Gao, T., Gu, R., … Xu, P. (2018). Draft genome of the protandrous Chinese black porgy, Acanthopagrus schlegelii. Gigascience, 7(4), giy012.
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(1971), 20212645.

Auteurs

Shuisheng Li (S)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

Wanshun Li (W)

BGI-Shenzhen, Shenzhen, China.

Shoujia Jiang (S)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.
Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, Shenzhen, China.

Yi Jing (Y)

BGI-Shenzhen, Shenzhen, China.
BGI-Sanya, BGI-Shenzhen, Sanya, China.

Ling Xiao (L)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Yangyang Yu (Y)

BGI Genomics, BGI-Shenzhen, Shenzhen, China.

Yun Liu (Y)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Yanhong Li (Y)

BGI Genomics, BGI-Shenzhen, Shenzhen, China.

Dengdong Wang (D)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Jiang Li (J)

BGI Genomics, BGI-Shenzhen, Shenzhen, China.

Cheng Peng (C)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Jiaxing Chen (J)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Danqi Lu (D)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.

Bin Wu (B)

BGI-Shenzhen, Shenzhen, China.

Xuanmin Guang (X)

BGI-Shenzhen, Shenzhen, China.

Junping Ma (J)

BGI Genomics, BGI-Shenzhen, Shenzhen, China.

Xinxin You (X)

Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, Shenzhen, China.

Yuqing Yang (Y)

Marine Fisheries Development Center of Guangdong Province, Huizhou, China.

Su Liu (S)

Marine Fisheries Development Center of Guangdong Province, Huizhou, China.

Xiaodong Fang (X)

BGI-Shenzhen, Shenzhen, China.

Qiang Gao (Q)

BGI Genomics, BGI-Shenzhen, Shenzhen, China.

Qiong Shi (Q)

Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, Shenzhen, China.

Haoran Lin (H)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

Manfred Schartl (M)

Developmental Biochemistry, University of Würzburg, Biozentrum, Am Hubland, Würzburg, and Comprehensive Cancer Center, University Clinic Würzburg, Würzburg, Germany.
Hagler Institute for Advanced Study and Department of Biology, Texas A&M University, College Station, Texas, USA.

Zhen Yue (Z)

BGI-Shenzhen, Shenzhen, China.
BGI-Sanya, BGI-Shenzhen, Sanya, China.

Yong Zhang (Y)

State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen University, Guangzhou, China.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

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