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Upregulation of the PPAR signaling pathway and accumulation of lipids are related to the morphological and structural transformation of the dragon-eye goldfish eye

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Abstract

Goldfish comprise around 300 different strains with drastically altered and aesthetical morphologies making them suitable models for evolutionary developmental biology. The dragon-eye strain is characterized by protruding eyes (analogous to those of Chinese dragons). Although the strain has been selected for about 400 years, the mechanism of its eye development remains unclear. In this study, a stable dragon-eye goldfish strain with a clear genetic background was rapidly established and studied. We found that upregulation of the PPAR signaling pathway accompanied by an increase in lipid accumulation might trigger the morphological and structural transformation of the eye in dragon-eye goldfish. At the developmental stage of proptosis (eye protrusion), downregulation of the phototransduction pathway was consistent with the structural defects and myopia of the dragon-eye strain. With the impairment of retinal development, cytokine-induced inflammation was activated, especially after proptosis, similar to the pathologic symptoms of many human ocular diseases. In addition, differentially expressed transcription factors were significantly enriched in the PAX and homeobox families, two well-known transcription factor families involved in eye development. Therefore, our findings reveal the dynamic changes in key pathways during eye development in dragon-eye goldfish, and provide insights into the molecular mechanisms underlying drastically altered eyes in goldfish and human ocular disease.

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References

  • Abe, G., Lee, S.H., Chang, M., Liu, S.C., Tsai, H.Y., and Ota, K.G. (2014). The origin of the bifurcated axial skeletal system in the twin-tail goldfish. Nat Commun 5, 3360.

    Article  PubMed  Google Scholar 

  • Abe, G., and Ota, K.G. (2017). Evolutionary developmental transition from median to paired morphology of vertebrate fins: Perspectives from twin-tail goldfish. Dev Biol 427, 251–257.

    Article  CAS  PubMed  Google Scholar 

  • Ashery-Padan, R., and Gruss, P. (2001). Pax6 lights-up the way for eye development. Curr Opin Cell Biol 13, 706–714.

    Article  CAS  PubMed  Google Scholar 

  • Bahn, R.S. (2010). Graves’ ophthalmopathy. N Engl J Med 362, 726–738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc-Ser B 57, 289–300.

    Google Scholar 

  • Blanco, A.M., Sundarrajan, L., Bertucci, J.I., and Unniappan, S. (2018). Why goldfish? Merits and challenges in employing goldfish as a model organism in comparative endocrinology research. Gen Comp Endocrinol 257, 13–28.

    Article  CAS  PubMed  Google Scholar 

  • Cabrera Blatter, M.F., del Prado, A., Gallelli, M.F., D’Anna, E., Ivanic, J., Esarte, M., Miceli, D.D., Gómez, N.V., and Castillo, V.A. (2012). Blindness in dogs with pituitary dependent hyperadrenocorticism: Relationship with glucose, cortisol and triglyceride concentration and with ophthalmic blood flow. Res Vet Sci 92, 387–392.

    Article  CAS  PubMed  Google Scholar 

  • Buchfink, B., Xie, C., and Huson, D.H. (2015). Fast and sensitive protein alignment using diamond. Nat Methods 12, 59–60.

    Article  CAS  PubMed  Google Scholar 

  • Candal, E., Ferreiro-Galve, S., Anadón, R., and Rodríguez-Moldes, I. (2008). Morphogenesis in the retina of a slow-developing teleost: Emergence of the GABAergic system in relation to cell proliferation and differentiation. Brain Res 1194, 21–27.

    Article  CAS  PubMed  Google Scholar 

  • Chang, C.H., Chiao, C.C., and Yan, H.Y. (2009). The structure and possible functions of the milkfish Chanos chanos adipose eyelid. J Fish Biol 75, 87–99.

    Article  PubMed  Google Scholar 

  • Chen, S.C. (1928). Transparency and mottling, a case of Mendelian inheritance in the goldfish Carassius auratus. Genetics 13, 434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, S.C. (1954). History of the domestication and the factors of the varietal formation of the common goldfish, Carassius auratus. Sci Sin 5, 287–321.

    Google Scholar 

  • Chen, Y., Chen, Y., Shi, C., Huang, Z., Zhang, Y., Li, S., Li, Y., Ye, J., Yu, C., Li, Z., et al. (2018). Soapnuke: A mapreduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data. GigaScience 7, gix120.

    Article  Google Scholar 

  • Chmurzyńska, A. (2006). The multigene family of fatty acid-binding proteins (fabps): Function, structure and polymorphism. J Appl Genet 47, 39–48.

    Article  PubMed  Google Scholar 

  • Choudhary, N.S., Kumar, N., and Duseja, A. (2019). Peroxisome proliferator-activated receptors and their agonists in nonalcoholic fatty liver disease. J Clin Exp Hepatol 9, 731–739.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cvekl, A., and Zhang, X. (2017). Signaling and gene regulatory networks in mammalian lens development. Trends Genet 33, 677–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeFelipe, J., López-Cruz, P.L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. (2013). New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14, 202–216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Easter Jr, S.S., and Hitchcock, P.F. (1986). The myopic eye of the black moor goldfish. Vision Res 26, 1831–1833.

    Article  PubMed  Google Scholar 

  • Fain, G.L., Hardie, R., and Laughlin, S.B. (2010). Phototransduction and the evolution of photoreceptors. Curr Biol 20, R114–R124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feldon, S.E., O’loughlin, C.W., Ray, D.M., Landskroner-Eiger, S., Seweryniak, K.E., and Phipps, R.P. (2006). Activated human T lymphocytes express cyclooxygenase-2 and produce proadipogenic prostaglandins that drive human orbital fibroblast differentiation to adipocytes. Am J Pathol 169, 1183–1193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu, Y. (1981). Initial viewpoint about the taxonomy of Chinese goldfish. Freshw Fish 6, 15–18.

    Google Scholar 

  • Furuhashi, M., Saitoh, S., Shimamoto, K., and Miura, T. (2014). Fatty acid-binding protein 4 (fabp4): Pathophysiological insights and potent clinical biomarker of metabolic and cardiovascular diseases. Clin Med Insights Cardiol 8s3, CMC.S17067.

    Article  Google Scholar 

  • Gao, F.X., Wang, Y., Zhang, Q.Y., Mou, C.Y., Li, Z., Deng, Y.S., Zhou, L., and Gui, J.F. (2017). Distinct herpesvirus resistances and immune responses of three gynogenetic clones of gibel carp revealed by comprehensive transcriptomes. BMC Genomics 18, 561.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gravina, A.G., Zagari, R.M., De Musis, C., Romano, L., Loguercio, C., and Romano, M. (2018). Helicobacter pylori and extragastric diseases: A review. World J Gastroenterol 24, 3204–3221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gui, J.F., and Zhou, L. (2010). Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci China Life Sci 53, 409–415.

    Article  PubMed  Google Scholar 

  • Ha, T.J., Swanson, D.J., Kirova, R., Yeung, J., Choi, K., Tong, Y., Chesler, E.J., and Goldowitz, D. (2012). Genome-wide microarray comparison reveals downstream genes of pax6 in the developing mouse cerebellum. Eur J Neurosci 36, 2888–2898.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harkewicz, R., Du, H., Tong, Z., Alkuraya, H., Bedell, M., Sun, W., Wang, X., Hsu, Y.H., Esteve-Rudd, J., Hughes, G., et al. (2012). Essential role of elovl4 protein in very long chain fatty acid synthesis and retinal function. J Biol Chem 287, 11469–11480.

    Article  CAS  PubMed  Google Scholar 

  • Hiromatsu, Y., Yang, D., and Bednarczuk, T. (2000). Cytokine profiles in eye muscle tissue and orbital fat tissue from patients with thyroid-associated ophthalmopathy. J Clin Endocrinol Metab 85, 1194–1199.

    CAS  PubMed  Google Scholar 

  • Huang, Z., Titus, T., Postlethwait, J.H., and Meng, F. (2019). Eye degeneration and loss of otx5b expression in the cavefish Sinocyclocheilus tileihornes. J Mol Evol 87, 199–208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johns, P.R., and Easter, S.S. (1977). Growth of the adult goldfish eye. II. Increase in retinal cell number. J Comp Neurol 176, 331–341.

    Article  CAS  PubMed  Google Scholar 

  • Kaneda, M., Nagashima, M., Nunome, T., Muramatsu, T., Yamada, Y., Kubo, M., Muramoto, K., Matsukawa, T., Koriyama, Y., Sugitani, K., et al. (2008). Changes of phospho-growth-associated protein 43 (phosphogap43) in the zebrafish retina after optic nerve injury: A long-term observation. Neurosci Res 61, 281–288.

    Article  CAS  PubMed  Google Scholar 

  • Khatol, P., Saraf, S., and Jain, A. (2018). Peroxisome proliferated activated receptors (PPARs): Opportunities and challenges for ocular therapy. Crit Rev Ther Drug Carrier Syst 35, 65–97.

    Article  PubMed  Google Scholar 

  • Kim, D., Paggi, J.M., Park, C., Bennett, C., and Salzberg, S.L. (2019). Graph-based genome alignment and genotyping with hisat2 and hisatgenotype. Nat Biotechnol 37, 907–915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kon, T., Omori, Y., Fukuta, K., Wada, H., Watanabe, M., Chen, Z., Iwasaki, M., Mishina, T., Matsuzaki, S.I.S., Yoshihara, D., et al. (2020). The genetic basis of morphological diversity in domesticated goldfish. Curr Biol 30, 2260–2274.e6.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., and Bahn, R.S. (2003). Relative overexpression of macrophage-derived cytokines in orbital adipose tissue from patients with Graves’ ophthalmopathy. J Clin Endocrinol Metab 88, 4246–4250.

    Article  CAS  PubMed  Google Scholar 

  • Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with bowtie 2. Nat Methods 9, 357–359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lantz, M., Vondrichova, T., Parikh, H., Frenander, C., Ridderstråle, M., Asman, P., Aberg, M., Groop, L., and Hallengren, B. (2005). Overexpression of immediate early genes in active Graves’ ophthalmopathy. J Clin Endocrinol Metab 90, 4784–4791.

    Article  CAS  PubMed  Google Scholar 

  • Li, B., and Dewey, C.N. (2011). Rsem: Accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, P. (1959). Phylogeny relationship of different breeds of Chinese goldfish. Chin J Zool 3, 248–251.

    Google Scholar 

  • Li, X.Y., and Gui, J.F. (2018a). Diverse and variable sex determination mechanisms in vertebrates. Sci China Life Sci 61, 1503–1514.

    Article  PubMed  Google Scholar 

  • Li, X.Y., and Gui, J.F. (2018b). An epigenetic regulatory switch controlling temperature-dependent sex determination in vertebrates. Sci China Life Sci 61, 996–998.

    Article  PubMed  Google Scholar 

  • Liu, Q., Qi, Y., Liang, Q., Xu, X., Hu, F., Wang, J., Xiao, J., Wang, S., Li, W., Tao, M., et al. (2018). The chimeric genes in the hybrid lineage of Carassius auratus cuvieri (♀)×Carassius auratus red var. (♂). Sci China Life Sci 61, 1079–1089.

    Article  PubMed  Google Scholar 

  • Liu, R.Z., Saxena, V., Sharma, M.K., Thisse, C., Thisse, B., Denovan-Wright, E.M., and Wright, J.M. (2007). The fabp4 gene of zebrafish (Danio rerio)—genomic homology with the mammalian FABP4 and divergence from the zebrafish fabp3 in developmental expression. FEBS J 274, 1621–1633.

    Article  CAS  PubMed  Google Scholar 

  • Lu, W.J., Gao, F.X., Wang, Y., Zhang, Q.Y., Li, Z., Zhang, X.J., Zhou, L., and Gui, J.F. (2019). Differential expression of innate and adaptive immune genes in the survivors of three gibel carp gynogenetic clones after herpesvirus challenge. BMC Genomics 20, 432.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma, D.M., Zhu, H.P., and Gui, J.F. (2008). Ectopic six3 expression in the dragon eye goldfish. Comp Biochem Physiol Part B-Biochem Mol Biol 149, 303–313.

    Article  Google Scholar 

  • Makowski, L., Boord, J.B., Maeda, K., Babaev, V.R., Uysal, K.T., Morgan, M.A., Parker, R.A., Suttles, J., Fazio, S., Hotamisligil, G.S., et al. (2001). Lack of macrophage fatty-acid-binding protein ap2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med 7, 699–705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marc, R.E., and Liu, W.L.S. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. J Comp Neurol 425, 560–582.

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Morales, J.R., Signore, M., Acampora, D., Simeone, A., and Bovolenta, P. (2001). Otx genes are required for tissue specification in the developing eye. Development (Cambridge, England) 128, 2019–2030.

    Article  CAS  Google Scholar 

  • Matsumura, M., Ohkuma, M., and Honda, Y. (1982). Retinal degeneration in celestial goldfish. Ophthalm Res 14, 344–353.

    Article  CAS  Google Scholar 

  • Mehlem, A., Hagberg, C.E., Muhl, L., Eriksson, U., and Falkevall, A. (2013). Imaging of neutral lipids by Oil Red O for analyzing the metabolic status in health and disease. Nat Protoc 8, 1149–1154.

    Article  PubMed  Google Scholar 

  • Miesfeld, J.B., and Brown, N.L. (2019). Eye organogenesis: A hierarchical view of ocular development. Current Topics in Developmental Biology 132, 351–393.

    Article  PubMed  Google Scholar 

  • Mimura, L.Y., Villares, S.M.F., Monteiro, M.L.R., Guazzelli, I.C., and Bloise, W. (2003). Peroxisome proliferator-activated receptor-γ gene expression in orbital adipose/connective tissues is increased during the active stage of Graves’ ophthalmopathy. Thyroid 13, 845–850.

    Article  CAS  PubMed  Google Scholar 

  • Mindel, J.S., and Rosenberg, E.W. (1997). Is heficobacter pylori of interest to ophthalmologists? Ophthalmology 104, 1729–1730.

    Article  CAS  PubMed  Google Scholar 

  • Mou, C.Y., Wang, Y., Zhang, Q.Y., Gao, F.X., Li, Z., Tong, J.F., Zhou, L., and Gui, J.F. (2018). Differential interferon system gene expression profiles in susceptible and resistant gynogenetic clones of gibel carp challenged with herpesvirus CaHV. Dev Comp Immunol 86, 52–64.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa, Y., Shiraki, T., Kojima, D., and Fukada, Y. (2015). Homeobox transcription factor six7 governs expression of green opsin genes in zebrafish. Proc R Soc B 282, 20150659.

    Article  PubMed  PubMed Central  Google Scholar 

  • Omori, Y., and Kon, T. (2019). Goldfish: An old and new model system to study vertebrate development, evolution and human disease. J Biochem 165, 209–218.

    Article  CAS  PubMed  Google Scholar 

  • Ota, K.G., and Abe, G. (2016). Goldfish morphology as a model for evolutionary developmental biology. WIREs Dev Biol 5, 272–295.

    Article  Google Scholar 

  • Pascual, G., Fong, A.L., Ogawa, S., Gamliel, A., Li, A.C., Perissi, V., Rose, D.W., Willson, T.M., Rosenfeld, M.G., and Glass, C.K. (2005). A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-γ. Nature 437, 759–763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.C., Mendell, J.T., and Salzberg, S.L. (2015). Stringtie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33, 290–295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popesku, J.T., Martyniuk, C.J., Mennigen, J., Xiong, H., Zhang, D., Xia, X., Cossins, A.R., and Trudeau, V.L. (2008). The goldfish (Carassius auratus) as a model for neuroendocrine signaling. Mol Cell Endocrinol 293, 43–56.

    Article  CAS  PubMed  Google Scholar 

  • Popova, E. (2015). Gabaergic neurotransmission and retinal ganglion cell function. J Comp Physiol A 201, 261–283.

    Article  CAS  Google Scholar 

  • Ramírez-Zacarías, J.L., Castro-Muñozledo, F., and Kuri-Harcuch, W. (1992). Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil Red O. Histochemistry 97, 493–497.

    Article  PubMed  Google Scholar 

  • Raymond, P., Spilman, D., Hill, R., and Bahn, C. (1984). The telescopic eyes of black moor goldfish: Elevated intraocular pressure and altered aqueous outflow pathways. Invest Ophthalmol Vis Sci 25, 282.

    Google Scholar 

  • Rosen, E.D., and MacDougald, O.A. (2006). Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7, 885–896.

    Article  CAS  PubMed  Google Scholar 

  • Saccà, S.C., Vagge, A., Pulliero, A., and Izzotti, A. (2014). Helicobacter pylori infection and eye diseases. Medicine 93, e216.

    Article  PubMed  PubMed Central  Google Scholar 

  • Saino-Saito, S., Nourani, R.M., Iwasa, H., Kondo, H., and Owada, Y. (2009). Discrete localization of various fatty-acid-binding proteins in various cell populations of mouse retina. Cell Tissue Res 338, 191–201.

    Article  CAS  PubMed  Google Scholar 

  • Salmerón, C. (2018). Adipogenesis in fish. J Exp Biol 221, jeb161588.

    Article  PubMed  Google Scholar 

  • Salmerón, C., Johansson, M., Angotzi, A.R., Rønnestad, I., Jönsson, E., Björnsson, B.T., Gutiérrez, J., Navarro, I., and Capilla, E. (2015). Effects of nutritional status on plasma leptin levels and in vitro regulation of adipocyte leptin expression and secretion in rainbow trout. Gen Comp Endocrinol 210, 114–123.

    Article  PubMed  Google Scholar 

  • Sandell, J.H., Martin, S.C., and Heinrich, G. (1994). The development of GABA immunoreactivity in the retina of the zebrafish (Brachydanio rerio). J Comp Neurol 345, 596–601.

    Article  CAS  PubMed  Google Scholar 

  • Seltner, R.L., Weerheim, J.A., and Sivak, J.G. (1989). Role of the lens and vitreous humor in the refractive properties of the eyes of three strains of goldfish. Vision Res 29, 681–685.

    Article  CAS  PubMed  Google Scholar 

  • Seritrakul, P., and Gross, J.M. (2019). Genetic and epigenetic control of retinal development in zebrafish. Curr Opin Neurobiol 59, 120–127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shichida, Y., and Matsuyama, T. (2009). Evolution of opsins and phototransduction. Phil Trans R Soc B 364, 2881–2895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivak, J.G., and Sivak, J.M. (2019). Conserved characteristics of ocular refractive development—Did the eye evolve once? Exp Eye Res 183, 84–87.

    Article  CAS  PubMed  Google Scholar 

  • Smartt, J. (2001). Goldfish Varieties and Genetics: Handbook for Breeders. (John Wiley & Sons), pp. 11–25.

  • Song, J., Zhong, C., Bonaguidi, M.A., Sun, G.J., Hsu, D., Gu, Y., Meletis, K., Huang, Z.J., Ge, S., Enikolopov, G., et al. (2012). Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489, 150–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, Y., Tao, B., Chen, J., Jia, S., Zhu, Z., Trudeau, V.L., and Hu, W. (2017). GABAergic neurons and their modulatory effects on gnrh3 in zebrafish. Endocrinology 158, 874–886.

    Article  CAS  PubMed  Google Scholar 

  • Sotolongo-Lopez, M., Alvarez-Delfin, K., Saade, C.J., Vera, D.L., and Fadool, J.M. (2016). Genetic dissection of dual roles for the transcription factor six7 in photoreceptor development and patterning in zebrafish. PLoS Genet 12, e1005968.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun, Z.H., Wang, Y., Lu, W.J., Li, Z., Liu, X.C., Li, S.S., Zhou, L., and Gui, J.F. (2017). Divergent expression patterns and function implications of four nanos genes in a hermaphroditic fish, epinephelus coioides. IJMS 18, 685.

    Article  PubMed Central  Google Scholar 

  • Tazaki, Y., Sugitani, K., Ogai, K., Kobayashi, I., Kawasaki, H., Aoyama, T., Suzuki, N., Tabuchi, Y., Hattori, A., and Kitamura, K.I. (2018). RANKL, Ephrin-Eph and Wnt10b are key intercellular communication molecules regulating bone remodeling in autologous transplanted goldfish scales. Comp Biochem Physiol Part A-Mol Integrat Physiol 225, 46–58.

    Article  CAS  Google Scholar 

  • Thieblemont, C., de la Fouchardière, A., and Coiffier, B. (2003). Nongastric mucosa-associated lymphoid tissue lymphomas. Clin Lymphoma 3, 212–224.

    Article  PubMed  Google Scholar 

  • Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with tophat and cufflinks. Nat Protoc 7, 562–578.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Den Brink, D.M., Cubizolle, A., Chatelain, G., Davoust, N., Girard, V., Johansen, S., Napoletano, F., Dourlen, P., Guillou, L., Angebault-Prouteau, C., et al. (2018). Physiological and pathological roles of fatp-mediated lipid droplets in Drosophila and mice retina. PLoS Genet 14, e1007627.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, L., Feng, Z., Wang, X., Wang, X., and Zhang, X. (2010). DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136–138.

    Article  PubMed  Google Scholar 

  • Wang, S.Y., Luo, J., Murphy, R.W., Wu, S.F., Zhu, C.L., Gao, Y., and Zhang, Y.P. (2013). Origin of Chinese goldfish and sequential loss of genetic diversity accompanies new breeds. PLoS ONE 8, e59571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye, Q., and Qu, L. (2017). Goldfish of China-descriptions and illustrations of diverse goldfish in China. (Fuzhou: The Straits Publishing & Distributing Group), pp. 19–27.

    Google Scholar 

  • Ying, X., Wai, M.S.M., Wang, Y., Lau, J.P.C., Forster, E.L., and Yew, D.T. (2009). Comparison of retinal degeneration in the normal goldfish and the megalophthalmic black moor goldfish after optic nerve transection and lens extraction. Int J Neurosci 119, 744–753.

    Article  Google Scholar 

  • Zhang, Q.Q., Zhou, L., Li, Z., Gan, R.H., Yu, Z.X., Gui, J.F., et al. (2020). Allelic diversification, syntenic alignment and expression patterns of nanos2 in polyploid gibel carp. Acta Hydrobiol Sin 44, 1087–1096.

    Google Scholar 

  • Zhang, Y., Sun, Y., Rao, E., Yan, F., Li, Q., Zhang, Y., Silverstein, K.A.T., Liu, S., Sauter, E., Cleary, M.P., et al. (2014). Fatty acid-binding protein E-FABP restricts tumor growth by promoting IFN-β responses in tumor-associated macrophages. Cancer Res 74, 2986–2998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, L., and Gui, J. (2017). Natural and artificial polyploids in aquaculture. Aquacult Fish 2, 103–111.

    Google Scholar 

  • Gui, J.F., Tang, Q., Li, Z., Liu, J., Silva, S.S. de. (2018). Aquaculture in China: success stories and modern trends. (John Wiley & Sons Ltd), pp. 149–157.

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Acknowledgements

This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000), the National Natural Science Foundation of China (31930111), the China Agriculture Research System (CARS-45-07), the Autonomous Project of the State Key Laboratory of Freshwater Ecology and Biotechnology (2019FBZ04). The research was supported by the Wuhan Branch, Supercomputing Centre, Chinese Academy of Sciences, China.

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Yu, P., Wang, Y., Yang, WT. et al. Upregulation of the PPAR signaling pathway and accumulation of lipids are related to the morphological and structural transformation of the dragon-eye goldfish eye. Sci. China Life Sci. 64, 1031–1049 (2021). https://doi.org/10.1007/s11427-020-1814-1

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