Kim et al. BMC Genomics (2018) 19:733 https://doi.org/10.1186/s12864-018-5079-x RESEARCHARTICLE Open Access A draft genome of the striped catfish, Pangasianodon hypophthalmus, for comparative analysis of genes relevant to development and a resource for aquaculture improvement Oanh T. P. Kim1*† , Phuong T. Nguyen1†, Eiichi Shoguchi2†, Kanako Hisata2, Thuy T. B. Vo1, Jun Inoue2, Chuya Shinzato2,4, Binh T. N. Le1, Koki Nishitsuji2, Miyuki Kanda3, Vu H. Nguyen1, Hai V. Nong1 and Noriyuki Satoh2* Abstract Background: The striped catfish, Pangasianodon hypophthalmus, is a freshwater and benthopelagic fish common in the Mekong River delta. Catfish constitute a valuable source of dietary protein. Therefore, they are cultured worldwide, and P. hypophthalmus is a food staple in the Mekong area. However, genetic information about the culture stock, is unavailable for breeding improvement, although genetics of the channel catfish, Ictalurus punctatus, has been reported. Toacquiregenomesequencedataasausefulresourcefor marker-assisted breeding, we decoded a draft genome of P. hypophthalmus and performed comparative analyses. Results: Using the Illumina platform, we obtained both nuclear and mitochondrial DNA sequences. Molecular phylogeny using the mitochondrial genome confirmed that P. hypophthalmus is a member of the family Pangasiidae and is nested within a clade including the families Cranoglanididae and Ictaluridae. The nuclear genome was estimated at approximately 700 Mb, assembled into 568 scaffolds with an N50 of 14.29 Mbp, and was estimated to contain ~ 28,600 protein-coding genes, comparable to those of channel catfish and zebrafish. Interestingly, zebrafish produce gadusol, but genes for biosynthesis of this sunscreen compound have been lost from catfish genomes. The differences in gene contents between these two catfishes were found in genes for vitamin D-binding protein and cytosolic phospholipase A2, which have lost only in channel catfish. The Hox cluster in catfish genomes comprised seven paralogous groups, similar to that of zebrafish, and comparative analysis clarified catfish lineage-specific losses of A5a, B10a, and A11a. Genes for insulin-like growth factor (IGF) signaling were conserved between the two catfish genomes. In addition to identification of MHC class I and sex determination- related gene loci, the hypothetical chromosomes by comparison with the channel catfish demonstrated the usefulness of the striped catfish genome as a marker resource. (Continued on next page) * Correspondence: [email protected]; [email protected] †Oanh T. P. Kim, Phuong T. Nguyen and Eiichi Shoguchi contributed equally to this work. 1Institute of Genome Research, Vietnam Academy of Science and Technology, Cau Giay, Hanoi, Vietnam 2Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. BMC Genomics (2018) 19:733 Page 2 of 16 (Continued from previous page) Conclusions: We developed genomic resources for the striped catfish. Possible conservation of genes for development and marker candidates were confirmed by comparing the assembled genome to that of a model fish, Danio rerio,and to channel catfish. Since the catfish genomic constituent resembles that of zebrafish, it is likely that zebrafish data for gene functions is applicable to striped catfish as well. Keywords: Striped catfish, Draft nuclear genome, Gadusol biosynthetic genes, Vitamin D-binding protein, cPLA2, Hox cluster, IGF, MHCI, Sex-determination genes, Hypothetical chromosome Background pancreatic necrosis (IPN) [ 25, 26]. Consequently, MAS has Catfish comprise approximately 4000 species belonging to been successfully used in the selection of IPN resistance in the teleost order Siluriformes [1]. They are globally distrib- Atlantic salmon, which can reduce the number of IPN out- uted in fresh, salty, and brackish water. Although catfish breaks by 75% in salmon farming [27]. have lost their scales evolutionarily, they occupy a phylo- Significant efforts have also been devoted to enhancing genetic position close to cyprinid fishes including the genomic and genetic research in other economically im- model fish, Danio rerio [2, 3]. Catfish are also an Ostario- portant aquaculture species, including catfish. The chan- physian species closely related to zebrafish and carp. nel catfish, I. punctatus, is cultured mostly in the U.S., Catfish constitute a valuable source of dietary protein [4] and its genome has been decoded [11, 17]. The channel and are therefore cultured worldwide as a leading aquacul- catfish genome identified genes relevant to the evolu- ture species [5–7]. The striped catfish, Pangasianodon tionary loss of scales in catfish although developmentally hypophthalmus Sauvage, 1878, is a freshwater and bentho- relevant genes and genes potentially relevant to aquacul- pelagic species that is common and widely cultured in the ture have not been analyzed in detail. In contrast, less Mekong River delta [7, 8]. Vietnam is the world’slargest genetic and genomic information has been reported in producer of P. hypophthalmus, with an estimated 1.1 mil- the striped catfish, P. hypophthalmus, which is widely lion tons being cultured on a farming area of more than cultured in the Mekong river delta. For example, Sri- 5000 ha [9, 10]. However, due to environmental changes phairoj et al. [28] were unable to construct sex-specific and other challenges, aquaculture methods and systems markers for Pangasianodon. Therefore, genomic re- must be constantly examined to improve production. Cat- sources of P. hypophthalmus are necessary to develop fishgenomicinformationmaybeusefultodevelop genome-based technologies for Asian catfish aquacul- marker-assisted breeding and associated genome-wide ana- ture. Moreover, P. hypophthalmus is naturally distrib- lyses for catfish aquaculture. uted in only the Chao Phraya river of Thailand and the Genomic information greatly facilitates fundamental re- Mekong river, which runs through Cambodia, Laos, search and applications for genetic improvement programs Thailand, and Vietnam. P. hypophthalmus migrates annu- in cultured species [11, 12]. The genomes of several eco- ally between spawning and feeding grounds. This species nomically important fish species have been sequenced, in- spawns in the upper reaches of the Cambodian Mekong cluding Atlantic cod (Gadus morhua)[13], rainbow trout River, then migrates back to the feeding grounds which are (Oncorhynchus mykiss)[14], Nile tilapia (Oreochromis nilo- located in the floodplain of Tonle Sap, central and lower ticus)[15], Atlantic salmon (Salmo salsar)[16], and chan- Mekong river and the Vietnamese Mekong delta [29]. Gen- nel catfish (Ictalurus punctatus)[17]. Using decoded etic diversity of P. hypophthalmus remains poorly under- genomes, researchers have analyzed polymorphic markers, stood. Only a few studies of population genetics have been linkage maps, and QTL/GWAS (Quantitative Trait Loci/ done for this species. However, findings are contradictory Genome-Wide Association Study). Results of these ana- because of the limited availability of genetic markers [30]. lyses can be used in breeding programs, including Genomic information about P. hypophthalmus is needed marker-assisted selection (MAS), genome selection (GS), for development of molecular markers that can be used in and genome editing. For example, genomic resources for genetic diversity and evolutionary studies. Atlantic salmon have been developed with whole-genome Here, we report the decoded genome of the striped cat- sequences [16] and 9.7 million non-redundant SNPs [18]. fish, P. hypophthalmus. We compare the striped catfish Moreover, a high-density genetic linkage map [19]anda genome to the channel catfish and zebrafish reference ge- number of QTL studies have characterized the correlation nomes, because striped catfish are phylogenetically closed between genetic and phenotypic variation, namely, QTLs to both. We also clarify the conservation of core deve- affecting flesh color and growth-related traits [20–22], late lopmental genes in each lineage. In addition, we try to sexual maturation [23], resistance to pancreatic disease construct hypothetical chromosomes by anchoring the (salmonid alphavirus) [24], and resistance to infectious striped catfish genome to channel catfish chromosomes as Kim et al. BMC Genomics (2018) 19:733 Page 3 of 16 a genome sequence resource, although the chromo- by Inoue et al. (2010) [35]. We confirmed that our spe- some number of the striped catfish has been reported cimen is P. hypophthalmus due to the almost identical as 2n = 60 [31], which is similar to that of channel sequence with that of P. hypophthalmus (NC_021752) catfish (2n = 58) [17]. shown by the short branch lengths between the two species (Fig. 1c). In addition, the clade belonging to P. Results hypophthalmus