Abstract
The Senegalese sole (Solea senegalensis, Kaup 1858) is a flatfish species of great value for aquaculture. In this study, we develop the first linkage map in this species based on microsatellite markers characterized from genomic DNA libraries and EST databases of Senegalese sole and from other flatfish species. Three reference gynogenetic families were obtained by chromosome-manipulation techniques: two haploid gynogenetics, used to assign and order microsatellites to linkage groups and another diploid gynogenetic family, used for estimating marker–centromere distances. The consensus map consists of 129 microsatellites distributed in 27 linkage groups (LG), with an average density of 4.7 markers per LG and comprising 1,004 centimorgans (cM). Additionally, 15 markers remained unlinked. Through half-tetrad analysis, we were able to estimate the centromere distance for 81 markers belonging to 24 LG, representing an average of 3 markers per LG. Comparative mapping was performed between flatfish species LG and model fish species chromosomes (stickleback, Tetraodon, medaka, fugu and zebrafish). The usefulness of microsatellite markers and the genetic map as tools for comparative mapping and evolution studies is discussed.
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Ahsan B, Kobayashi D, Yamada T, Kasahara M, Sasaki S, Saito TLN, Nagayasu Y, Doi K, Nakatani Y, Qu W (2008) UTGB/medaka: genomic resource database for medaka biology. Nucleic Acids Res 36:D747–D752
Aliah RS, Taniguchi N (2000) Gene-centromere distances of six microsatellite DNA loci in gynogenesis Nishikigoi (Cyprinus carpio). Fish Genetics and Breeding Science 29:113–119
Aparicio S, Chapman J, Stupka E, Putnam N, Chia J, Dehal P, Christoffels A, Rash S, Hoon S, Smit A (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310
Arijo S, Rico R, Chabrillon M, Diaz-Rosales P, Martínez-Manzanares E, Balebona MC, Magariños B, Toranzo AE, Moriñigo MA (2005) Effectiveness of a divalent vaccine for sole, Solea senegalensis (Kaup), against Vibrio harveyi and Photobacterium damselae subsp. piscicida. J Fish Dis 28:33–38
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
Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, McPherson JD, Johnson SL (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10:1351–1358
Bouza C, Sanchez L, Martínez P (1994) Karotypic characterization of turbot (Scophthalmus maximus) with conventional, fluorochrome and restriction endonuclease-banding techniques. Mar Biol 120:609–613
Bouza C, Presa P, Castro J, Sánchez L, Martínez P (2002) Allozyme and microsatellite diversity in natural and domestic populations of turbot (Scophthalmus maximus) in comparison with other Pleuronectiformes. J Fish Aquat Sci Can 59:1460–1473
Bouza C, Hermida M, Pardo BG, Fernández C, Fortes GG, Castro J, Sánchez L, Presa P, Pérez M, Sanjuán A, de Carlos A, Alvarez-Dios JÁ, Ezcurra S, Cal RM, Piferrer F, Martínez P (2007) A microsatellite genetic map of the turbot (Scophthalmus maximus). Genetics 177:2457–2467
Bouza C, Hermida M, Millán A, Vilas R, Vera M, Fernández C, Calaza M, Pardo BG, Martínez P (2008) Characterization of EST-derived microsatellites for gene mapping and evolutionary genomics in turbot. Anim Genet 39:666–670
Bouza C, Hermida M, Pardo BG, Vera M, Fernández C, de la Herrán R, Navajas-Pérez R, Álvarez-Dios JA, Gómez-Tato A, Martínez P (2012) An expressed sequence tag (EST)-enriched genetic map of turbot (Scophthalmus maximus): a useful framework for comparative genomics across model and farmed teleosts. BMC Genet 13:54
Cabrita E, Soares F, Dinis MT (2006) Characterization of Senegalese sole, Solea senegalensis, male broodstock in terms of sperm production and quality. Aquaculture 261:967–975
Castaño-Sánchez C, Fuji K, Ozaki A, Hasegawa O, Sakamoto T, Morishima K, Nakayama I, Fujiwara A, Masaoka T, Okamoto H, Hayashida K, Tagami M, Kawai J, Hayashizaki Y, Okamoto N (2010) A second generation genetic linkage map of Japanese flounder (Paralichthys olivaceus). BMC Genomics 11:554
Castro J, Pino A, Hermida M, Bouza C, Riaza A, Ferreiro I, Sánchez L, Martínez P (2006) A microsatellite marker tool for parentage analysis in Senegal sole (Solea senegalensis): genotyping errors, null alleles and conformance to theoretical assumptions. Aquaculture 261:1194–1203
Cerdà J, Mercadé J, Lozano JJ, Manchado M, Tingaud-Sequeira A, Astola A, Infante C, Halm S, Viñas J, Castellana B (2008) Genomic resources for a commercial flatfish, the Senegalese sole (Solea senegalensis): EST sequencing, oligo microarray design, and development of the Soleamold bioinformatic platform. BMC Genomics 9:508
Cerdà J, Douglas S, Reith M (2010) Genomic resources for flatfish research and their applications. J Fish Biol 77:1045–1070
Chen SL, Ma HY, Jiang Y, Liao XL, Meng L (2007) Isolation and characterization of polymorphic microsatellite loci from an EST library of turbot (Scophthalmus maximus) and cross-species amplification. Mol Ecol Notes 7:848–850
Chen SL, Shao C-W, Xu GB, Liao XL, Tian YS (2008) Development of 15 novel dinucleotide microsatellite markers in the Senegalese sole Solea senegalensis. Fish Sci 74:1357–1359
Chen SL, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff JN, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Qi, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 3(46):253-60
Chistiakov DA, Tsigenopoulos CS, Lagnel J, Guo YM, Hellemans B, Haley CS, Volckaert FAM, Kotoulas G (2008) A combined AFLP and microsatellite linkage map and pilot comparative genomic analysis of European sea bass Dicentrarchus labrax L. Anim Genet 39:623–634
Choo KHA (1998) Why is the centromere so cold? Genome Res 8:81–82
Coimbra MRM, Hasegawa O, Kobayashi K, Koretsugu S, Ohara E, Okamoto N (2001) Twenty microsatellite markers from the Japanese flounder Paralichthys olivaceus. Fish Sci 67:358–360
Coimbra MRM, Kobayashi K, Koretsugu S, Hasegawa O, Ohara E, Ozaki A, Sakamoto T, Naruse K, Okamoto N (2003) A genetic linkage map of the Japanese. Aquaculture 220:203–218
Coughlan J, McCarthy E, McGregor D, O'Donoghue P, Galvin P, Fitzgerald R, Daemen E, Imsland A, Stefansson S, Cross T (1996) Four polymorphic microsatellites in turbot Scophthalmus maximus. Anim Genet 27:441
Cristescu MEA, Colbourne JK, Radivojac J, Lynch M (2006) A microsatellite-based genetic linkage map of the waterflea, Daphnia pulex: on the prospect of crustacean genomics. Genomics 88:415–430
Danzmann RG, Gharbi K (2001) Gene mapping in fishes: a means to an end. Genetica 111:3–23
De La Herrán R, Robles F, Navas JI, Hamman-Khalifa AM, Herrera M, Hachero I, Mora MJ, Ruiz Rejón C, Garrido-Ramos M, Ruiz Rejón M (2008) A highly accurate, single PCR reaction for parentage assignment in Senegal sole based on eight informative microsatellite loci. Aquac Res 39:1169–1174
Diaz-Ferguson E, Cross I, Barrios M, Pino A, Castro J, Bouza C, Martinez P, Rebordinos L (2012) Genetic characterization, based on microsatellite loci, of Solea senegalensis (Soleidae, Pleuronectiformes) in Atlantic coast populations of the SW Iberian Peninsula. Cienc Mar 38:129–142
Díaz-Rosales P, Arijo S, Chabrillón M, Alarcón FJ, Tapia-Paniagua ST, Martínez-Manzanares E, Moriñigo MA (2009) Effects of two closely related probiotics on respiratory burst activity of Senegalese sole (Solea senegalensis, Kaup) phagocytes, and protection against Photobacterium damselae subsp. piscicida. Aquaculture 293:16–21
Douglas SE, Knickle LC, Kimball J, Reith ME (2007) Comprehensive EST analysis of Atlantic halibut (Hippoglossus hippoglossus), a commercially relevant aquaculture species. BMC Genomics 8:144
Fernandez-Trujillo MA, Bejar J, Gallardo JB, Porta JM, Borrego JJ, Mendez T, Alvarez MC (2007) Molecular cloning and characterization of C-type lysozyme from Senegalese sole (Solea senegalensis). Aquaculture 272:S255
Fortes G (2008) Desarrollo de un mapa genético con marcadores AFLPs y microsatélites en rodaballo (Scopthalmus maximus L.). Thesis doctoral Universidad de Santiago de Compostela
Franch R, Louro B, Tsalavouta M, Chatziplis D, Tsigenopoulos CS, Sarropoulou E, Antonello J, Magoulas A, Mylonas CC, Babbucci M, Patarnello T, Power DM, Kotoulas G, Bargelloni L (2006) A genetic linkage map of the hermaphrodite teleost fish Sparus aurata L. Genetics 174:851–861
Funes V, Zuasti E, Catanese G, Infante C, Manchado M (2004) Isolation and characterization of ten microsatellite loci for Senegal sole (Solea senegalensis Kaup). Mol Ecol Notes 4:339–341
García-Cegarra A, Merlo M, 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. Cytogenet Genome Res 141:227–240
Gavaia P, Dinis M, Cancela M (2002) Osteological development and abnormalities of the vertebral column and caudal skeleton in larval and juvenile stages of hatchery-reared Senegal sole (Solea senegalensis). Aquaculture 211:305–323
Gilbey J, Verspoor E, McLay A, Houlihan D (2004) A microsatellite linkage map for Atlantic salmon (Salmo salar). Anim Genet 35:98–105
Guyomard R, Mauger S, Tabet-Canale K, Martineau S, Genet C, Krieg F, Quillet E (2006) A type I and type II microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) with presumptive coverage of all chromosome arms. BMC Genomics 7:302
Guyon R, Rakotomanga M, Azzouzi N, Coutanceau JP, Bonillo C, D’Cotta H, Pepey E, Soler L, Rodier-Goud M, D’Hont A, Conte MA, van Bers NEM, Penman DJ, Hitte C, Crooijmans RPMA, Kocher TD, Ozouf-Costaz C, Baroiller J, Galibert F (2012) A high-resolution map of the Nile tilapia genome: a resource for studying cichlids and other percomorphs. BMC Genomics 13:222
Guzmán JM, Cal R, García-López A, Chereguini O, Kight K, Olmedo M, Sarasquete C, Mylonas CC, Peleteiro JB, Zohar Y, Mañanós EL (2011) Effects of in vivo treatment with the dopamine antagonist pimozide and gonadotropin-releasing hormone agonist (GnRHa) on the reproductive axis of Senegalese sole (Solea senegalensis). Comp Biochem Physiol A Mol Integr Physiol 158:235–245
Hermida M, Bouza C, Fernández C, Sciara A, Rodríguez-Ramilo ST, Fernández J, Martínez P (2013) Compilation of mapping resources in turbot (Scophthalmus maximus): a new integrated consensus genetic map. Aquaculture 414:19–25
Hermida M, Rodríguez-Ramilo ST, Hachero-Cruzado I, Herrera M, Sciara AA, Bouza C, Fernández J, Martínez P (2014) First genetic linkage map for comparative mapping and QTL screening of brill (Scophthalmus rhombus). Aquaculture. doi:10.1016/j.aquaculture.2013.02.041
Hinegardner R (1968) Evolution of cellular DNA content in teleost fishes. Am Nat 102:517–523
Hinegardner R, Rosen DE (1972) Cellular DNA content and the evolution of teleostean fishes. Am Nat 106:621–644
Hufton AL, Groth D, Vingron M, Lehrach H, Poustka AJ, Panopoulou G, Vingron M (2008) Early vertebrate whole genome duplications were predated by a period of intense genome rearrangement. Genome Res 18:1582–1591
Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fish 13:379–408
Infante C, Ponce M, Manchado M (2011) Duplication of calsequestrin genes in teleosts: molecular characterization in the Senegalese sole (Solea senegalensis). Comp Biochem Physiol B Biochem Mol Biol 158:304–314
Iyengar A, Piyapattanakorn S, Heipel DA, Stone DM, Howell BR, Child AR, MacLean N (2000) A suite of highly polymorphic microsatellite markers in turbot (Scophthalmus maximus L.) with potential for use across several flatfish species. Mol Ecol 9:368–371
Jaillon O, Aury J-M, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biémont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigó R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quétier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957
Ji XS, Chen SL, Liao XL, Yang JF, Xu TJ, Ma HY, Tian YS, Jiang YL, Wu P (2009) Microsatellite-centromere mapping in Cynoglossus semilaevis using gynogenetic diploid families produced by the use of homologous and non-homologous sperm. J Fish Biol 75:422–434
Johnson SL, Gates MA, Johnson M, Talbot WS, Horne S, Baik K, Rude S, Wong JR, Postlewait JH (1996) Centromere-linkage analysis and consolidation of the zebrafish genetic map. Genetics 142:1277–1288
Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, Birney E, Searle S, Schmutz J, Grimwood J, Dickson MC, Myers RM, Miller CT, Summers BR, Knecht AK, Brady SD, Zhang H, Pollen AA, Howes T, Amemiya C, Baldwin J, Bloom T, Jaffe DB, Nicol R, Wilkinson J, Lander ES, Di Palma F, Lindblad-Toh K, Kingsley DM (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61
Kai W, Kikuchi K, Fujita M, Suetake H, Fujiwara A, Yoshiura Y, Ototake M, Venkatesh B, Miyaki K, Suzuki Y (2005) A genetic linkage map for the tiger pufferfish, Takifugu rubripes. Genetics 171:227–238
Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, Hosoya S, Suetake H, Naruse K, Brenner S, Suzuki Y, Venkatesh B (2011) Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals. Genome Biol Evol 3:424–442
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
Kang J-H, Kim W-J, Lee W-J (2008) Genetic linkage map of olive flounder, Paralichthys olivaceus. Int J Biol Sci 4:143–149
Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y, Jindo T, Kobayashi D, Shimada A, Toyoda A, Kuroki Y, Fujiyama A, Sasaki T, Shimizu A, Asakawa S, Shimizu N, Hashimoto SI, Yang J, Lee Y, Matsushima K, Sugano S, Sakaizumi M, Narita T, Ohishi K, Haga S, Ohta F, Nomoto H, Nogata K, Morishita T, Endo T, Shin-I T, Takeda H, Morishita S, Kohara Y (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714–719
Kauffman EJ, Gestl EE, Kim DJ, Walker C, Hite JM, Yan G, Rogan PK, Johnson SL, Cheng KC (1995) Microsatellite–centromere mapping in the zebrafish (Danio rerio). Genomics 30:337–341
Kelly PD, Chu F, Woods IG, Ngo-Hazelett P, Cardozo T, Huang H, Kimm F, Liao L, Yan Y-L, Zhou Y, Johnson SL, Abagyan R, Schier AF, Postlethwait JH, Talbot WS (2000) Genetic linkage mapping of zebrafish genes and ESTs. Genome Res 10:558–567
Kim DS, Cheong SC, Park SR, Lee JK (1988) Cytogenetic and biochemical studies on the flatfish, Paralichthys olivaceus. Bull Natl Fish Res Dev Agency (Korea) Yangsan 42:135–142
Kocher TD, Lee WJ, Sobolewska H, Penman D, Mcandrew B (1998) A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148:1225–1232
Kosambi DD (1994) The estimation of map distances from recombination values. Ann Eugenics 12:172–175
Kucuktas H, Wang S, Li P, He C, Xu P, Sha Z, Liu H, Jiang Y, Baoprasertkul P, Somridhivej B, Wang Y, Abernathy J, Guo X, Liu L, Muir W, Liu Z (2009) Construction of genetic linkage maps and comparative genome analysis of catfish using gene-associated markers. Genetics 181:1649–1660
Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD (2005) A second-generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237–244
Li Q, Kijima A (2005) Segregation of microsatellite alleles in gynogenetic diploid Pacific abalone (Haliotis discus hannai). Mar Biotechnol 7:669–676
Li Q, Kijima A (2006) Gynogenetic tetraploid larvae of the Pacific oyster Crassostrea gigas induced by inhibition of the 1st and 2nd meiotic divisions. Tohoku J Agric Res 57(1/2):1–10
Lie O, Slettan A, Lingaas F, Olsaker I, Hordvik I, Refstie T (1994) Haploid gynogenesis: a powerful strategy for linkage analysis in fish. Anim Biotechnol 5:33–45
Lindner KR, Seeb JE, Habicht C, Knudsen KL, Kretschmer E, Reedy DJ, Spruell P, Allendorf FW (2000) Gene–centromere mapping of 312 loci in pink salmon by half-tetrad analysis. Genome NRC 43:538–549
Liu YG, Sun XQ, Gao H, Liu LX (2007) Microsatellite markers from an expressed sequence tag library of half-smooth tongue sole (Cynoglossus semilaevis) and their application in other related fish species. Mol Ecol Notes 7:1242–1244
Martínez P, Hermida M, Pardo BG, Fernández C, Castro J, Cal RM, Álvarez-Dios JA, Gómez-Tato A, Bouza C (2008) Centromere-linkage in the turbot (Scophthalmus maximus) through half-tetrad analysis in diploid meiogynogenetics. Aquaculture 280:81–88
Massault C, Franch R, Haley C, De Koning DJ, Bovenhuis H, Pellizzari C, Patarnello T, Bargelloni L (2010a) Quantitative trait loci for resistance to fish pasteurellosis in gilthead sea bream (Sparus aurata). Anim Genet 42:191–203
Massault C, Hellemans B, Louro B, Batargias C, Van Houdt JKJ, Canario A, Volckaert FAM, Bovenhuis H, Haley C, De Koning DJ (2010b) QTL for body weight, morphometric traits and stress response in European sea bass Dicentrarchus labrax. Anim Genet 41:337–345
Matsuoka MP, Gharrett AJ, Wilmot RL, Smoker WW (2004) Gene–centromere distances of allozyme loci in even- and odd-year pink salmon (Oncorhynchus gorbuscha). Genetica 121:1–11
Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138
Molina-Luzón MJ, López JR, Navajas-Pérez R, Robles F, Ruiz-Rejón C, De La Herrán R (2012) Validation and comparison of microsatellite markers derived from Senegalese sole (Solea senegalensis, Kaup) genomic and expressed sequence tags libraries. Mol Ecol Resour 12:956–966
Molina-Luzón MJ, López JR, Robles F, Navajas-Pérez R, Ruiz-Rejón C, De la Herrán R, Navas JI (2014) Chromosomal manipulation in Senegalese sole (Solea senegalensis Kaup, 1858): induction of triploidy and gynogenesis. J Appl Genetics. Doi:10-1007/s13353-014-0233-x
Navajas-Pérez R, Robles F, Molina-Luzón MJ, De La Herrán R, Alvarez-Dios JA, Pardo BG, Vera M, Bouza C, Martínez P (2012) Exploitation of a turbot (Scophthalmus maximus L.) immune-related expressed sequence tag (EST) database for microsatellite screening and validation. Mol Ecol Resour 12:706–716
Nomura K, Morishima K, Tanaka H, Unuma T, Okuzawa K, Ohta H, Arai K (2006) Microsatellite–centromere mapping in the Japanese eel (Anguilla japonica) by half-tetrad analysis using induced triploid families. Aquaculture 257:53–67
Ooijen JW, Voorrips R E (2002) JoinMap: version 3.0: software for the calculation of genetic linkage maps. University and Research Center
Ødegård J, Baranski M, Gjerde B, Gjedrem T (2011) Methodology for genetic evaluation of disease resistance in aquaculture species: challenges and future prospects. Aquacult Res 42:103–114
Pardo BG, Fernández C, Hermida M, Vázquez-López A, Pérez M, Presa P, Calaza M, Alvarez-Dios JA, Comesaña AS, Raposo-Guillán J, Bouza C, Martínez P (2007) Development and characterization of 248 novel microsatellite markers in turbot (Scophthalmus maximus). Genome NRC 50:329–332
Pardo BG, Fernández C, Millán A, Bouza C, Vázquez-López A, Vera M, Alvarez-Dios JA, Calaza M, Gómez-Tato A, Vázquez M, Cabaleiro S, Magariños B, Lemos ML, Leiro JM, Martínez P (2008) Expressed sequence tags (ESTs) from immune tissues of turbot (Scophthalmus maximus) challenged with pathogens. BMC Vet Res 4:37
Pérez F, Ortiz J, Zhinaula M, Gonzabay C, Calderón J, Volckaert FAMJ (2005) Development of EST-SSR markers by data mining in three species of shrimp: Litopenaeus vannamei: Litopenaeus vannamei, Litopenaeus stylirostris, and Trachypenaeus birdy. Mar Biotechnol 7:554–569
Ponce M, Salas-Leiton E, Garcia-Cegarra A, Boglino A, Coste O, Infante C, Gisbert E, Rebordinos L, Manchado M (2011) Genomic characterization, phylogeny and gene regulation of g-type lysozyme in sole (Solea senegalensis). Fish Shellfish Immunol 31:925–937
Poompuang S, Na-Nakorn U (2004) A preliminary genetic map of walking catfish (Clarias macrocephalus). Aquaculture 232:195–203
Porta J, Alvarez MC (2004) Development and characterization of microsatellites from Senegal sole (Solea Senegalensis). Mol Ecol Notes 4:277–279
Porta J, Porta JM, Martínez-Rodríguez G, del Carmen Alvarez M (2006a) Development of a microsatellite multiplex PCR for Senegalese sole (Solea senegalensis) and its application to broodstock management. Aquaculture 256:159–166
Porta J, Porta JM, Martínez-Rodríguez G, del Carmen Alvarez M (2006b) Genetic structure and genetic relatedness of a hatchery stock of Senegal sole (Solea senegalensis) inferred by microsatellites. Aquaculture 251:46–55
Postlethwait JH, Johnson SL, Midson CN, Talbot WS, Gates M, Ballinger EW, Africa D, Andrews R, Carl T, Eisen JS (1994) A genetic linkage map for the zebrafish. Science 264:699–703
Prat F (2004) Pleurogene: El Primer Proyecto de Genómica de Peces en España. Instituto de Acuicultura de Torre de la Sal (IATS).Consejo Superior de Investigaciones Científicas (CSIC). http://www.uv.es/rvgp/reunion2004/Prat.pdf
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reid DP, Szanto A, Glebe B, Danzmann RG, Ferguson MM (2004) QTL for body weight and condition factor in Atlantic salmon (Salmo salar): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Arctic charr (Salvelinus alpinus). Heredity 94:166–172
Reid DP, Smith C-A, Rommens M, Blanchard B, Martin-Robichaud D, Reith M (2007) A genetic linkage map of Atlantic halibut (Hippoglossus hippoglossus L.). Genetics 177:1193–1205
Rexroad CE, Rodriguez MF, Coulibaly I, Gharbi K, Danzmann RG, Dekoning J, Phillips R, Palti Y (2005) Comparative mapping of expressed sequence tags containing microsatellites in rainbow trout (Oncorhynchus mykiss). BMC Genomics 6:54
Rodríguez-Ramilo ST, Toro MA, Bouza C, Hermida M, Pardo BG, Cabaleiro S, Martínez P, Fernández J (2011) QTL detection for Aeromonas salmonicida resistance related traits in turbot (Scophthalmus maximus). BMC Genomics 12:541
Rodríguez-Ramilo ST, De La Herrán R, Ruiz-Rejón C, Hermida M, Fernández C, Pereiro P, Figueras A, Bouza C, Toro MA, Martínez P (2013) Identification of quantitative trait loci associated with resistance to viral haemorrhagic septicaemia (VHS) in turbot (Scophthalmus maximus): a comparison between bacterium, parasite and virus diseases. Mar Biotechnol. doi:10.1007/s10126-013-9544-x
Ruan X, Wang W, Kong J, Yu F, Huang X (2010) Genetic linkage mapping of turbot (Scophthalmus maximus L.) using microsatellite markers and its application in QTL analysis. Aquaculture 308:89–100
Ruan X, Wang W, Kong J, Hu J (2011) Isolation and analysis of microsatellites in the genome of turbot (Scophthalmus maximus L.). Afr J Biotechnol 10:507–518
Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467
Sarropoulou E, Fernandes JMO (2011) Comparative genomics in teleost species: knowledge transfer by linking the genomes of model and non-model fish species. CompBiochem Physiol D Genomics Proteomics 6:92–102
Sarropoulou E, Nousdili D, Magoulas A, Kotoulas G (2008) Linking the genomes of nonmodel teleosts through comparative genomics. Mar Biotechnol 10:227–233
Sato T, Yokomizo S, Matsuda M, Hamaguchi S, Sakaizumi M (2001) Gene–centromere mapping of medaka sex chromosomes using triploid hybrids between Oryzias latipes and O. luzonensis. Genetica 111:71–75
Schoen DJ (2000) Comparative genomics, marker density and statistical analysis of chromosome rearrangements. Genetics 154:943–952
Sémon M, Wolfe KH (2007) Rearrangement rate following the whole-genome duplication in teleosts. Mol Biol Evol 24:860–867
Sha Z, Wang S, Zhuang Z, Wang Q, Li P, Ding H, Wang N, Liu Z, Chen S (2010) Generation and analysis of 10 000 ESTs from the half-smooth tongue sole Cynoglossus semilaevis and identification of microsatellite and SNP markers. J Fish Biol 76:1190–1204
Slettan A, Olsaker I, Lie O (1997) Segregation studies and linkage analysis of Atlantic salmo microsatellites using haploid genetics. Heredity 78:620–627
Soares F, Engrola S, Dinis MT (2002) Anomalías en la pigmentación de juveniles de lenguado (Solea senegalensis). Bol Inst Esp Oceanogr 18:405–407
Steinke D, Hoegg S, Brinkmann H, Meyer A (2006) Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol 4:16
Stemshorn KC, Nolte AW, Tautz D (2005) A genetic map of Cottus gobio (Pisces, Teleostei) based on microsatellites can be linked to the physical map of Tetraodon nigroviridis. J Evol Biol 18:1619–1624
Sun XW, Liang LQ (2004) A genetic linkage map of common carp (Cyprinus carpio L.) and mapping of a locus associated with cold tolerance. Aquaculture 238:165–172
Thorgaard GH, Allendorf FW, Knudsen KL (1983) Gene–centromere mapping in rainbow trout: high interference over long map distances. Genetics 103:771–783
Vega L, Díaz E, Cross I, Rebordinos L (2002) Caracterizaciones citogenética e isoenzimática del lenguado Solea senegalensis Kaup, 1858. Bol Inst Esp Oceanogr 18(1–4):245–250
Vera M, Álvarez-Dios JA, Millán A, Pardo BG, Bouza C, Hermida M, Fernández C, De la Herrán R, Molina-Luzón MJ, Martínez P (2011) Validation of single nucleotide polymorphism (SNP) markers from an immune expressed sequence tag (EST) turbot, Scophthalmus maximus, database. Aquaculture 313:31–41
Villalta M, Estévez A, Bransden MP (2005) Arachidonic acid enriched live prey induces albinism in Senegal sole (Solea senegalensis) larvae. Aquaculture 245:193–209
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Waldbieser GC, Bosworth BG, Nonneman DJ, Wolters WR (2001) A microsatellite-based genetic linkage map for channel catfish, Ictalurus punctatus. Genetics 158:727–734
Wang CM, Zhu ZY, Lo LC, Feng F, Lin G, Yang WT, Li J, Yue GH (2007) A microsatellite linkage map of Barramundi, Lates calcarifer. Genetics 175:907–915
Wang CM, Bai ZY, He XP, Lin G, Xia JH, Sun F, Lo LC, Feng F, Zhu ZY, Yue GH (2011) A high-resolution linkage map for comparative genome analysis and QTL fine mapping in Asian seabass, Lates calcarifer. BMC Genomics 12:174
Williams CG (1998) QTL mapping in outbreed pedigrees. In: Paterson AH (ed) Molecular dissection of complex traits. CRC Press, New York, pp 81–95
Zorrilla I, Arijo S, Chabrillon M, Diaz P, Martinez-Manzanares E, Balebona MC, Moriñigo MA (2003) Vibrio species isolated from diseased farmed sole, Solea senegalensis (Kaup), and evaluation of the potential virulence role of their extracellular products. J Fish Dis 26:103–108
Acknowledgments
This work has been supported by the Spanish Ministry of Science and Innovation (AGL2009-11872), Pleurogene-Flatfish Genomics and the Consolider-Ingenio AQUAGENOMICS Project (CSD2007-00002).
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Molina-Luzón, M.J., Hermida, M., Navajas-Pérez, R. et al. First Haploid Genetic Map Based on Microsatellite Markers in Senegalese Sole (Solea senegalensis, Kaup 1858). Mar Biotechnol 17, 8–22 (2015). https://doi.org/10.1007/s10126-014-9589-5
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DOI: https://doi.org/10.1007/s10126-014-9589-5