Genetic Basis for Eye Migration in Flatfish

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Flatfish Metamorphosis
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Abstract

Eye migration involves two aspects: which eye prefers to migrate upward and how far it migrates. We hypothesized that the genetic control of which way the eye prefers to migrate is already in place during early embryonic stages, when the eyes start forming. Several SNPs of genes involved in the control of eye development were investigated by comparing the neurula transcriptomes of the starry flounder and Japanese flounder. How far the eye migrates may be related to the duplication of TRβ, and a new copy of TRβb showed correlative expression with eye movement during Japanese flounder metamorphosis.

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References

  • Aritaki M, Seikai T (2004) Temperature effects on early development and occurrence of metamorphosis related morphological abnormalities in hatchery reared brown sole Pseudopleuronectes herzensteini. Aquaculture 240:517–530

    Article  Google Scholar 

  • Aydin I (2012) The external abnormalities of hatchery-reared Black Sea flounder (Platichthys flesus luscus Pallas, 1984) in Turkey. Turk J Fish Aquat Sci 12:127–133

    Article  Google Scholar 

  • Aydin Ì, Küҫük E, Sahin T, Kumlu M (2015) Effect of temperature on reversed asymmetry in hatchery-reared flounder (Platichthys flesus luscus Pallas, 1811). Turkish J Fish Aquat Sci 15:1–2

    Google Scholar 

  • Babcock LE (2005) Asymmetry in the fossil record. Eur Rev 13:135–143

    Article  Google Scholar 

  • Bao B, Ke Z, **ng J, Peatman E, Liu Z, **e C, Xu B, Gai J, Gong X, Yan G, Jiang Y, Tang W, Ren D (2011) Proliferating cells in suborbital tissue drive eye migration in flatfish. Dev Biol 351:200–207

    Article  CAS  Google Scholar 

  • Bao B, Yang G, Liu Z, Li S, Wang Z, Ren D (2005) Isolation of SFRS3 gene and its differential expression during metamorphosis involving eye migration of Japanese flounder Paralichthys olivaceus. Biochim Biophys Acta 1725:64–70

    Article  CAS  Google Scholar 

  • Benetti DD, Grabe SW, Feeley MW, Stevens OM, Powell TM, Leingang AJ, Main KL (2001) Development of aquaculture methods for southern flounder, Paralichthys lethostigma: I. Spawning and larval culture. J Appl Aquac 11:113–133

    Article  Google Scholar 

  • Bi S, Zheng Z, Lin R (1987) A preliminary study on the reversal of the flatfish (Pseudopleuronectes yokohame Günther). J Fish China 11(2):93–99

    Google Scholar 

  • Bisbal GA, Bengtson DA (1993) Reversed asymmetry in laboratory-reared summer flounder. Progressive Fish-Culturist 55:106–108

    Article  Google Scholar 

  • Chen J, 2015. Genes screening on the polymorphism of eye position in flatfishes (Pleuronectiformes). Master thesis of Shanghai Ocean University

    Google Scholar 

  • Chen J, Bao B (2015) Expression of pax6, tbx3 and rx1 gene during embryonic development in flounder (Paralichthys olivaceus). J Shanghai Ocean Univ 24(3):321–325. (abstract in English)

    CAS  Google Scholar 

  • Concha ML, Wilson SW (2001) Asymmetry in the epithalamus of vertebrates. J Anat 199:63–84

    Article  CAS  Google Scholar 

  • Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210(1-4):285–304

    Article  CAS  Google Scholar 

  • England SJ, Blanchard GB, Mahadevan L, Adams RJ (2006) A dynamic fate map of the forebrain shows how vertebrate eyes form and explains two causes of cyclopia. Development 133:4613–4617

    Article  CAS  Google Scholar 

  • Femández I, Ortiz-Delgado JB, Darias MJ, Hontoria F, Andree KB, Manchado M, Sarasquete C, Gisbert E (2017) Vitamin a affects flatfish development in a thyroid hormone signaling and metamorphic stage dependent manner. Front Physiol 8:458

    Article  Google Scholar 

  • Galay-Burgos M, Power DM, Llewellyn L, Sweeney GE (2008) Thyroid hormone receptor expression during metamorphosis of Atlantic halibut (Hippoglossus hippoglossus). Mol Cell Endocrinol 281:56–63

    Article  CAS  Google Scholar 

  • García-Angulo A, Merlo MA, Iziga R, Rodríguez ME, Portela-Bens S, Al-Rikabi A, Liehr T, Rebordinos L (2020) Gene clusters related to metamorphosis in Solea senegalensis are highly conserved. Comp Biochem Physiol, Part D: Genomics Proteomics 35:100706

    Google Scholar 

  • Hamada H, Meno C, Watanabe D, Saijoh Y (2002) Establishment of vertebrate left-right asymmetry. Nat Rev Genet 3:103–113

    Article  CAS  Google Scholar 

  • Hashimoto H, Aritaki M, Uozumi K, Uji S, Kurokawa T, Suzuki T (2007) Embryogenesis and expression profiles of charon and nodal-pathway genes in sinistral (Paralichthys olivaceus) and dextral (Verasper variegatus) flounders. Zool Sci 24:137–146

    Article  CAS  Google Scholar 

  • Hashimoto H, Mizuta A, Okada N, Suzuki T (2001) Japanese flounder, reversed, displays a randomization of metamorphic and visceral left-right asymmetries without correlation. Fish Sci 68(2):1301–1302

    Google Scholar 

  • Hashimoto H, Mizuta A, Okada N, Suzuki T, Tagawa M, Tabata K, Yoshihiro Y, Sakaguchi M, Tanaka M, Toyohara H (2002) Isolation and characterization of a Japanese flounder clonal line, reversed, which exhibits reversal of metamorphic left-right asymmetry. Mech Dev 111:17–24

    Article  CAS  Google Scholar 

  • Huang L, Li G, Mo Z, **ao P, Li J, Huang J (2015) De novo assembly of the Japanese flounder (Paralichthys olivaceus) spleen transcriptome to identify putative genes involved in immunity. PLoS One 10:e0117642

    Article  Google Scholar 

  • Inui Y, Miwa S (1985) Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol 60(3):450–454

    Article  CAS  Google Scholar 

  • Isorna E, Obregon MJ, Calvo RM, Vázquez R, Pendón C, Falcón J, Muñoz-Cueto JA (2009) Iodothyronine deiodinases and thyroid hormone receptors regulation during flatfish (Solea senegalensis) metamorphosis. J Exp Zool B Mol Dev Evol 312B:231–246

    Article  CAS  Google Scholar 

  • Itoh K, Watanabe K, Wu X, Suzuki T (2010) Three members of the iodothyronine deiodinase family, dio1, dio2 and dio3, are expressed in spatially and temporally specific patterns during metamorphosis of the flounder, Paralichthys olivaceus. Zoolog Sci 27(7):574–580

    Article  CAS  Google Scholar 

  • Kang D, Lee J, Kim W, Kim H (2012) Morphological specificity in cultured starry flounder Platichthys stellatus reared in artificial facility. Fish Aquat Sci 15(2):117–123

    Google Scholar 

  • Klaren PHM, Wunderink YS, Yu’Fera M, Mancera JM, Flik G (2008) The thyroid gland and thyroid hormones in Senegalese sole (Solea senegalensis) during early development and metamorphosis. Gen Comp Endocrinol 155:686–694

    Article  CAS  Google Scholar 

  • Kuan YS, Gamse JT, Schreiber AM, Halpern ME (2007) Selective asymmetry in a conserved forebrain to midbrain projection. J Exp Zool, Part B 308:669–678

    Article  Google Scholar 

  • Levin M (2005) Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122:3–25

    Article  CAS  Google Scholar 

  • Li L, Zheng J, Bao B, Berendzen PB (2013) Change of eye shape during metamorphosis in two flatfishes, Paralichthys olivaceus and Solea senegalensis, with comparison of eye shape within the Pleuronectiformes. Ichthyol Res 60:178–183

    Article  CAS  Google Scholar 

  • Liu K, Chen S, Zhang L, Dong Z, Li H, Liu W (2014) Molecular cloning and expression of thyroid hormone receptors β gene (TRβ) from half-smooth tongue sole (Cynoglossus semilaevis). J Agric Biotechnol 22(9):1157–1165

    CAS  Google Scholar 

  • Palmer AR (2004) Symmetry breaking and the evolution of development. Science 306:828–833

    Article  CAS  Google Scholar 

  • Policansky D (1982) Flatfishes and the inheritance of asymmetries. Behav Brain Sci 5:262–265

    Article  Google Scholar 

  • Rembold M, Loosli F, Adams RJ, Wittbrodt J (2006) Individual cell migration serves as the driving force for optic vesicle evagination. Science 313:1130–1134

    Article  CAS  Google Scholar 

  • Sawayama E (2019) Identification of an SNP marker associated with abnormal eye location in Japanese flounder based on genome-wide analysis. Marine Biotechnology Conference, Shizuoka, Japan

    Google Scholar 

  • Schreiber AM (2006) Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. J Exp Biol 209(4):610–621

    Article  Google Scholar 

  • Schreiber AM (2013) Flatfish: an asymmetric perspective on metamorphosis. In: Shi Y-B (ed) Current topics in developmental biology, vol 103. Academic Press, Burlington, pp 167–194

    Google Scholar 

  • Schreiber AM, Specker JL (1998) Metamorphosis in the summer flounder (Paralichthys dentatus): stage-specific development response to altered thyroid status. Gen Comp Endocrinol 111:156–166

    Article  CAS  Google Scholar 

  • Seikai T, Matsumot J, Shimozaki M, Oikawa A, Akiyama T (1987) An association of melanophores appearing at metamorphosis as vehicles of asymmetric skin color formation with pigment anomalies developed under hatchery conditions in the Japanese flounder, Paralichthys olivaceus. Pigment Cell Res 1(3):143–151

    Article  CAS  Google Scholar 

  • Shao C, Bao B, **e 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 AM, Wang N, Wei F, Zhang J, Dong Z, Gao L, Gai J, Sakamoto T, Mo S, Chen W, Shi Q, Li H, **u Y, Li Y, Xu W, Shi Z, Zhang G, Power DM, Wang Q, Schartl M, Chen S (2017) The genome and transcriptome of Japanese flounder provide insights into flatfish asymmetry. Nat Genet 49:119–124

    Article  CAS  Google Scholar 

  • Si Y, Li H, Gong X, Bao B (2021) Isolation of prolactin gene and its differential expression during metamorphosis involving eye migration of Japanese flounder Paralichthys olivaceus. Gene 780:145522

    Article  CAS  Google Scholar 

  • Sinn R, Wittbrodt J (2013) An eye on eye development. Mech Dev 130(2013):347–358

    Article  CAS  Google Scholar 

  • Snelson CD, Gamse JT (2009) Building an asymmetric brain: development of the zebrafish epithalamus. Semin Cell Dev Biol 20:491–497

    Article  Google Scholar 

  • Soffientino B, Specker JL (2001) Metamorphosis of summer flounder, Paralichthys dentatus: cell proliferation and differentiation of the gastric mucosa a developmental effects of altered thyroidal status. J Exp Zool 290:31–40

    Article  CAS  Google Scholar 

  • Sun M, Wei F, Li H, Xu J, Chen X, Gong X, Tian Y, Chen S, Bao B (2015) Distortion of frontal bones results from cell apoptosis by the mechanical force from the up-migrating eye during metamorphosis in Paralichthys olivaceus. Mech Dev 136:87–98

    Article  CAS  Google Scholar 

  • Suzuki T, Washio Y, Aritaki M, Fu**ami Y, Shimizu D, Uji S, Hashimoto H (2009) Metamorphic pitx2 expression in the left habenula correlated with lateralization of eye sidedness in flounder. Develop Growth Differ 51:797–808

    Article  CAS  Google Scholar 

  • Tagawa M, Aritaki M (2005) Production of symmetrical flatfish by controlling the timing of thyroid hormone treatment in spotted halibut Verasper variegatus. Gen Comp Endocrinol 141:184–189

    Article  CAS  Google Scholar 

  • Tong Y, Sun X, Wang B, Wang L, Li Y, Tian J, Zheng F, Zheng M (2014) Transcriptome of intraperitoneal organs of starry flounder Platichthys stellatus challenged by Edwardsiella ictaluri JCM1680. Chin J Oceanol Limnol 33:20–27

    Article  Google Scholar 

  • Wang W, Wang J, You F, Ma L, Yang X, Gao J, He Y, Qi J, Yu H, Wang Z, Wang X, Wu Z, Zhang Q (2014) Detection of alternative splice and gene duplication by RNA sequencing in Japanese flounder, Paralichthys olivaceus. G3 4:2419–2424

    Article  Google Scholar 

  • Wei F, Chen J, Chen X, Bao B (2017) Comparative analysis with the neurula transcriptomes of two species of flatfishes Platichthys stellatus and Paralichthys olivaceus. Gene 596:147–153

    Article  CAS  Google Scholar 

  • **e C, Xu S, Yang L, Ke Z, Jiang Y, **ng J, Gong X, Xu L, Bao B (2011) mRNA/microRNA profile at metamorphic stage of Oliver flounder, Paralichthys olivaceus. Comp Funct Genomics 2011:1–12

    Article  Google Scholar 

  • **ng J, Ke Z, Liu L, Li C, Gong X, Bao B (2020) Eye location, cranial asymmetry, and swimming behavior of different variants of Solea senegalensis. Aquacult Fish 5:182–186. https://doi.org/10.1016/j.aaf.2019.11.003

    Article  Google Scholar 

  • Yamano K, Araki K, Sekikawa K, Inui Y (1994) Cloning of thyroid hormone receptor genes expressed in metamorphosing flounder. Dev Genet 15(4):378–382

    Article  CAS  Google Scholar 

  • Yamano K, Inui Y (1995) cDNA cloning of thyroid hormone receptor b for the Japanese flounder. Gen Comp Endocrinol 99:197–203

    Article  CAS  Google Scholar 

  • Yamano K, Miwa S (1998) Differential gene expression of thyroid hormone receptor alpha and beta in fish development. Gen Comp Endocrinol 109:75–85

    Article  CAS  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18(6):292–298

    Article  Google Scholar 

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Bao, B. (2022). Genetic Basis for Eye Migration in Flatfish. In: Flatfish Metamorphosis. Springer, Singapore. https://doi.org/10.1007/978-981-19-7859-3_9

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