Dataset Information

Genomic Characterization of hox Genes in Senegalese Sole (Solea senegalensis, Kaup 1858): Clues to Evolutionary Path in Pleuronectiformes.

ABSTRACT: The Senegalese sole (Solea senegalensis, Kaup 1858), a marine flatfish, belongs to the Pleuronectiformes order. It is a commercially important species for fisheries and aquaculture. However, in aquaculture, several production bottlenecks have still to be resolved, including skeletal deformities and high mortality during the larval and juvenile phase. The study aims to characterize the hox gene clusters in S. senegalensis to understand better the developmental and metamorphosis process in this species. Using a BAC library, the clones that contain hox genes were isolated, sequenced by NGS and used as BAC-FISH probes. Subsequently the hox clusters were studied by sequence analysis, comparative genomics, and cytogenetic and phylogenetic analysis. Cytogenetic analysis demonstrated the localization of four BAC clones on chromosome pairs 4, 12, 13, and 16 of the Senegalese sole cytogenomic map. Comparative and phylogenetic analysis showed a highly conserved organization in each cluster and different phylogenetic clustering in each hox cluster. Analysis of structural and repetitive sequences revealed accumulations of polymorphisms mediated by repetitive elements in the hoxba cluster, mainly retroelements. Therefore, a possible loss of the hoxb7a gene can be established in the Pleuronectiformes lineage. This work allows the organization and regulation of hox clusters to be understood, and is a good base for further studies of expression patterns.

SUBMITTER: Mendizabal-Castillero M

PROVIDER: S-EPMC9774920 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Genomic Characterization of hox Genes in Senegalese Sole (Solea senegalensis, Kaup 1858): Clues to Evolutionary Path in Pleuronectiformes.

Mendizábal-Castillero Marco M Merlo Manuel Alejandro MA Cross Ismael I Rodríguez María Esther ME Rebordinos Laureana L

Animals : an open access journal from MDPI 20221219 24

The Senegalese sole (Solea senegalensis, Kaup 1858), a marine flatfish, belongs to the Pleuronectiformes order. It is a commercially important species for fisheries and aquaculture. However, in aquaculture, several production bottlenecks have still to be resolved, including skeletal deformities and high mortality during the larval and juvenile phase. The study aims to characterize the hox gene clusters in S. senegalensis to understand better the developmental and metamorphos ...[more]

PMID: 36552509

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Project description:The retinas of nonmammalian vertebrates have cone photoreceptor mosaics that are often organized as highly patterned lattice-like distributions. In fishes, the two main lattice-like patterns are composed of double cones and single cones that are either assembled as interdigitized squares or as alternating rows. The functional significance of such orderly patterning is unknown. Here, the cone mosaics in two species of Soleidae flatfishes, the common sole and the Senegalese sole, were characterized and compared to those from other fishes to explore variability in cone patterning and how it may relate to visual function. The cone mosaics of the common sole and the Senegalese sole consisted of single, double, and triple cones in formations that differed from the traditional square mosaic pattern reported for other flatfishes in that no evidence of higher order periodicity was present. Furthermore, mean regularity indices for single and double cones were conspicuously lower than those of other fishes with "typical" square and row mosaics, but comparable to those of goldfish, a species with lattice-like periodicity in its cone mosaic. Opsin transcripts detected by quantitative polymerase chain reaction (sws1, sws2, rh2.3, rh2.4, lws, and rh1) were uniformly expressed across the retina of the common sole but, in the Senegalese sole, sws2, rh2.4, and rh1 were more prevalent in the dorsal retina. Microspectrophotometry revealed five visual pigments in the retina of the common sole [S(472), M(523), M(536), L(559), and rod(511)] corresponding to the repertoire of transcripts quantified except for sws1. Overall, these results indicate a loss of cone mosaic patterning in species that are primarily nocturnal or dwell in low light environments as is the case for the common sole and the Senegalese sole. The corollary is that lattice-like patterning of the cone mosaic may improve visual acuity. Ecological and physiological correlates derived from observations across multiple fish taxa that live in low light environments and do not possess lattice-like cone mosaics are congruent with this claim.

Project description:BackgroundKeratins make up the largest subgroup of intermediate filaments, and, in chordates, represent the most abundant proteins in epithelial cells. They have been associated with a wide range of functions in the cell, but little information is still available about their expression profile and regulation during flatfish metamorphosis. Senegalese sole (Solea senegalensis) is a commercially important flatfish in which no keratin gene has been described yet.ResultsThe development of large-scale genomics of Senegalese sole has facilitated the identification of two different type I keratin genes referred to as sseKer1 and sseKer2. Main characteristics and sequence identities with other fish and mammal keratins are described. Phylogenetic analyses grouped sseKer1 and sseKer2 in a significant clade with other teleost epidermal type I keratins, and have allowed for the identification of sseKer2 as a novel keratin. The expression profile of both genes was studied during larval development and in tissues using a real-time approach. sseKer1 and sseKer2 mRNA levels were significantly higher in skin than in other tissues examined. During metamorphosis, sseKer1 transcripts increased significantly at first stages, and reduced thereafter. In contrast, sseKer2 mRNA levels did not change during early metamorphosis although a significant drop at metamorphosis climax and late metamorphosis was also detected. To study the possible regulation of sseKer gene expressions by thyroid hormones (THs), larvae were exposed to the goitrogen thiourea (TU). TU-treated larvae exhibited higher sseKer1 and sseKer2 mRNA levels than untreated control at both 11 and 15 days after treatment. Moreover, addition of exogenous T4 hormone to TU-treated larvae restored or even reduced the steady-state levels with respect to the untreated control, demonstrating that expression of both genes is negatively regulated by THs.ConclusionWe have identified two keratin genes, referred to as sseKer1 and sseKer2, in Senegalese sole. Phylogenetic analyses revealed sseKer2 as a novel keratin. Although they exhibit different expression patterns during larval development, both of them are negatively regulated by THs. The co-regulation by THs could explain the reduction of both keratin transcripts after the metamorphosis climax, suggesting their role in the tissue remodelling processes that occur during metamorphosis.

Project description:BACKGROUND: Senegalese sole (Solea senegalensis) and common sole (S. solea) are two economically and evolutionary important flatfish species both in fisheries and aquaculture. Although some genomic resources and tools were recently described in these species, further sequencing efforts are required to establish a complete transcriptome, and to identify new molecular markers. Moreover, the comparative analysis of transcriptomes will be useful to understand flatfish evolution. RESULTS: A comprehensive characterization of the transcriptome for each species was carried out using a large set of Illumina data (more than 1,800 millions reads for each sole species) and 454 reads (more than 5 millions reads only in S. senegalensis), providing coverages ranging from 1,384x to 2,543x. After a de novo assembly, 45,063 and 38,402 different transcripts were obtained, comprising 18,738 and 22,683 full-length cDNAs in S. senegalensis and S. solea, respectively. A reference transcriptome with the longest unique transcripts and putative non-redundant new transcripts was established for each species. A subset of 11,953 reference transcripts was qualified as highly reliable orthologs (>97% identity) between both species. A small subset of putative species-specific, lineage-specific and flatfish-specific transcripts were also identified. Furthermore, transcriptome data permitted the identification of single nucleotide polymorphisms and simple-sequence repeats confirmed by FISH to be used in further genetic and expression studies. Moreover, evidences on the retention of crystallins crybb1, crybb1-like and crybb3 in the two species of soles are also presented. Transcriptome information was applied to the design of a microarray tool in S. senegalensis that was successfully tested and validated by qPCR. Finally, transcriptomic data were hosted and structured at SoleaDB. CONCLUSIONS: Transcriptomes and molecular markers identified in this study represent a valuable source for future genomic studies in these economically important species. Orthology analysis provided new clues regarding sole genome evolution indicating a divergent evolution of crystallins in flatfish. The design of a microarray and establishment of a reference transcriptome will be useful for large-scale gene expression studies. Moreover, the integration of transcriptomic data in the SoleaDB will facilitate the management of genomic information in these important species.

Dataset Information

Genomic Characterization of hox Genes in Senegalese Sole (Solea senegalensis, Kaup 1858): Clues to Evolutionary Path in Pleuronectiformes.

Publications

Genomic Characterization of <i>hox</i> Genes in Senegalese Sole (<i>Solea senegalensis</i>, Kaup 1858): Clues to Evolutionary Path in Pleuronectiformes.

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