fmars-06-00760 December 6, 2019 Time: 15:34 # 1 ORIGINAL RESEARCH published: 20 December 2019 doi: 10.3389/fmars.2019.00760 Genome Sequencing and Transcriptome Analysis Reveal Recent Species-Specific Gene Duplications in the Plastic Gilthead Sea Bream (Sparus aurata) Jaume Pérez-Sánchez1*, Fernando Naya-Català1, Beatriz Soriano2, M. Carla Piazzon3, Ahmed Hafez2, Toni Gabaldón4, Carlos Llorens2, Ariadna Sitjà-Bobadilla3 and Josep A. Calduch-Giner1 1 Nutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la Sal (IATS), Consejo Superior de Investigaciones Científicas, Castellón de la Plana, Spain, 2 Biotechvana, Parc Cientific, Universitat de València, Valencia, Spain, 3 Fish Pathology Group, Institute of Aquaculture Torre de la Sal (IATS), Consejo Superior de Investigaciones Científicas, Ribera de Cabanes, Castellón de la Plana, Spain, 4 Bioinformatics and Genomics Unit, Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain Gilthead sea bream is an economically important fish species that is remarkably well- Edited by: Jianhua Fan, adapted to farming and changing environments. Understanding the genomic basis East China University of Science of this plasticity will serve to orientate domestication and selective breeding toward and Technology, China more robust and efficient fish. To address this goal, a draft genome assembly was Reviewed by: reconstructed combining short- and long-read high-throughput sequencing with genetic Dongmei Wang, Ocean University of China, China linkage maps. The assembled unmasked genome spans 1.24 Gb of an expected Laura Ghigliotti, 1.59 Gb genome size with 932 scaffolds (∼732 Mb) anchored to 24 chromosomes Consiglio Nazionale delle Ricerche, Italy that are available as a karyotype browser at www.nutrigroup-iats.org/seabreamdb. *Correspondence: Homology-based functional annotation, supported by RNA-seq transcripts, identified Jaume Pérez-Sánchez 55,423 actively transcribed genes corresponding to 21,275 unique descriptions with [email protected] more than 55% of duplicated genes. The mobilome accounts for the 75% of the full Specialty section: genome size and it is mostly constituted by introns (599 Mb), whereas the rest is This article was submitted to represented by low complexity repeats, RNA retrotransposons, DNA transposons, and Marine Biotechnology, non-coding RNAs. This mobilome also contains a large number of chimeric/composite a section of the journal Frontiers in Marine Science genes (i.e., loci presenting fragments or exons mostly surrounded by LINEs and Received: 16 September 2019 Tc1/mariner DNA transposons), whose analysis revealed an enrichment in immune- Accepted: 22 November 2019 related functions and processes. Analysis of synteny and gene phylogenies uncovered a Published: 20 December 2019 high rate of species-specific duplications, resulting from recent independent duplications Citation: Pérez-Sánchez J, Naya-Català F, rather than from genome polyploidization (2.024 duplications per gene; 0.385 excluding Soriano B, Piazzon MC, Hafez A, gene expansions). These species-specific duplications were enriched in gene families Gabaldón T, Llorens C, functionally related to genome transposition, immune response, and sensory responses. Sitjà-Bobadilla A and Calduch-Giner JA (2019) Genome Additionally, transcriptional analysis of liver, skeletal muscle, intestine, gills, and spleen Sequencing and Transcriptome supported a high number of functionally specialized paralogs under tissue-exclusive Analysis Reveal Recent Species-Specific Gene Duplications regulation. Altogether, these findings suggest a role of recent large-scale gene in the Plastic Gilthead Sea Bream duplications coupled to tissue expression diversification in the evolution of gilthead (Sparus aurata). sea bream genome during its successful adaptation to a changing and pathogen- Front. Mar. Sci. 6:760. doi: 10.3389/fmars.2019.00760 rich environment. This issue also underscores a role of evolutionary routes for rapid Frontiers in Marine Science| www.frontiersin.org 1 December 2019| Volume 6| Article 760 fmars-06-00760 December 6, 2019 Time: 15:34 # 2 Pérez-Sánchez et al. Gilthead Sea Bream Genome Duplications increase of the gene repertoire in teleost fish that are independent of polyploidization. Since gilthead sea bream has a well-recognized plasticity, the current study will advance our understanding of fish biology and how organisms of this taxon interact with the environment. Keywords: gilthead sea bream, phylogenomics, gene duplications, transposon mobilization, immune response, response to stimulus, adaptive plasticity INTRODUCTION 2005), a third event of WGD (3R) occurred in the genome of the ancestor of teleost fish that is still present in the Gilthead sea bream (Sparus aurata) is a temperate marine coastal signature of modern teleost genomes (Jaillon et al., 2004; finfish that belongs to the Sparidae family, order Perciformes. It Kasahara et al., 2007). More recent WGD events occurred at is an economically important species highly cultured throughout the common ancestor of cyprinids and salmonids (Macqueen the Mediterranean area with a yearly production of more and Johnston, 2014; Chen et al., 2019). Comparative genomic than 218,000 metric tonnes, mostly concentrated in Turkey, analyses have shown that, generally, WGDs are followed by Greece, Egypt, and Spain (FAO, 2019). It occurs naturally in the massive and rapid genomic reorganizations driving the retention Mediterranean and the Eastern Atlantic Seas, from the British of a small proportion of duplicated genes (Langham et al., Isles and Strait of Gibraltar to Cape Verde and Canary Islands, 2004). However, recent studies in rainbow trout (Oncorhynchus supporting previous studies of genetic structure a strong genetic mykiss) reveal that the rediploidization process can be stepwise subdivision between Atlantic and Mediterranean populations and slower than expected (Berthelot et al., 2014). Further (Alarcón et al., 2004; De Innocentiis et al., 2004). Intriguingly, complexity comes from tandemly-arrayed genes that are critical strong subdivisions have also been found at short distances zones of adaptive plasticity, forming the building blocks for along the Tunisian coasts (Ben Slimen et al., 2004) or between more versatile immune, reproductive and sensory responses the French and Algerian coasts (Chaoui et al., 2009). However, in plants and animals including fish (Rizzon et al., 2006; unconstrained gene flow occurs along the coast of Italy, in the Kliebenstein, 2008; Van der Aa et al., 2009; Lu et al., absence of physical and ecological barriers between the Adriatic 2012). In any case, it has been shown that retained genes and Mediterranean Seas (Franchini et al., 2012). following WGDs or small scale duplicates are preferentially Gilthead sea bream is a protandrous hermaphrodite species, associated with species-specific adaptive traits (Maere et al., as it matures as male during its first and second years, but 2005). This notion is reinforced by the recently published most individuals change to females between their second to study of large-scale ruminant genome comparisons (Chen fourth year of life (Zohar et al., 1978). This sexual dimorphism et al., 2019), also evidenced in the case of modern teleosts is a fascinating subject in evolutionary biology, and Pauletto and primitive eels (Chen et al., 2008; Tine et al., 2014; et al.(2018) showed for the first time in a hermaphrodite Rozenfeld et al., 2019) for their improved adjustment to vertebrate species that the evolutionary pattern of sex-biased natural environment. genes is highly divergent when compared to what is observed Here we produced a high quality draft sequence of the gilthead in gonochoristic species. The ecological plasticity of gilthead sea bream genome by combining high-throughput sequencing sea bream is evidenced by the wide range of temperature (5– with genetic linkage maps. Synteny and phylogenomic analyses ◦ 33 C) and salinity (3–70 ) that is able to inhabit (Kleszczynska´ of the assembled genes revealed a high frequency of species- et al., 2006; Ortega, 2008h). These eurythermal and euryhaline specific duplications, mostly resulting in the enrichment characteristics, in combination with a notable resilience to of biological processes related to genome transposition but aquaculture stressors, make this species a rather unique fish also to immune response and sensory responses. RNA-seq with a high plasticity to farming and challenging environments. transcriptional analysis supported a divergent regulation and This adaptation to varying culture conditions has been assessed function of the multiple copies of tissue-exclusive genes. These in a number of physiological studies with focus on nutrition results highlight the gilthead sea bream as an interesting model (Benedito-Palos et al., 2016; Simó-Mirabet et al., 2018; Gil- to assess the teleost genome expansion and its contribution to Solsona et al., 2019), chronobiology (Mata-Sotres et al., 2015; adaptive plasticity in a challenging environment. Yúfera et al., 2017), feeding behavior (López-Olmeda et al., 2009; Sánchez et al., 2009), stress (Calduch-Giner et al., 2010; Castanheira et al., 2013; Pérez-Sánchez et al., 2013; Bermejo- MATERIALS AND METHODS Nogales et al., 2014; Magnoni et al., 2017; Martos-Sitcha et al., 2017, 2019), or disease resilience (Cordero et al., 2016; Ethics Statement Estensoro et al., 2016; Piazzon et al., 2018; Simó-Mirabet et al., Procedures for fish manipulation and tissue