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- A thyroid hormone regulated asymmetric responsive centre is correlated with eye migration during flatfish metamorphosisPublication . Campinho, Marco António; Silva, Nádia; Martins, Gabriel G.; Anjos, Liliana; Florindo, Claudia; Roman-Padilla, Javier; Garcia-Cegarra, Ana; Louro, Bruno; Manchado, Manuel; Power, DeborahFlatfish metamorphosis is a unique post-embryonic developmental event in which thyroid hormones (THs) drive the development of symmetric pelagic larva into asymmetric benthic juveniles. One of the eyes migrates to join the other eye on the opposite side of the head. Developmental mechanisms at the basis of the acquisition of flatfish anatomical asymmetry remain an open question. Here we demonstrate that an TH responsive asymmetric centre, determined by deiodinase 2 expression, ventrally juxtaposed to the migrating eye in sole (Solea senegalensis) correlates with asymmetric cranial ossification that in turn drives eye migration. Besides skin pigmentation that is asymmetric between dorsal and ventral sides, only the most anterior head region delimited by the eyes becomes asymmetric whereas the remainder of the head and organs therein stay symmetric. Sub-ocular ossification is common to all flatfish analysed to date, so we propose that this newly discovered mechanism is universal and is associated with eye migration in all flatfish.
- Having a BLAST: searchable transcriptome resources for the gilthead sea bream and the European sea bassPublication . Louro, Bruno; Marques, João Pedro; Power, Deborah; Canário, Adelino V. M.The gilthead sea bream (Sparus aurata) and the European sea bass (Dicentrarchus labrax) are the most important aquaculture species in the Mediterranean Sea and since the last decade it has been seen an exponential increase in their available molecular resources. In order to improve accessibility to transcriptome resources, Expressed Sequence Tags (ESTs), mRNA sequences and raw read sequences were assembled and deposited in BLAST queryable databases. The publicly available sea bream and sea bass sequences (6.4 and 247.5 million) generated 45,094 and 68,117 assembled sequences, with, respectively, arithmetic mean size of 998 and 2125 bp and N50 of 1302 and 2966 bp. The assemblies will be regularly updated and new analytical tools added to the web server at http://sea.ccmar.ualg.pt. (C) 2016 Elsevier B.V. All rights reserved.
- Heritability of cortisol response to confinement stress in European sea bass dicentrarchus labraxPublication . Volckaert, F.; Hellemans, Bart; Batargias, C.; Louro, Bruno; Massault, C.; Van Houdt, Jeroen K. J.; Haley, Chris; De Koning, Dirk-Jan; Canario, Adelino V. M.In fish, the most studied production traits in terms of heritability are body weight or growth, stress or disease resistance, while heritability of cortisol levels, widely used as a measure of response to stress, is less studied. In this study, we have estimated heritabilities of two growth traits (body weight and length) and of cortisol response to confinement stress in the European sea bass.FindingsThe F1 progeny analysed (n = 922) belonged to a small effective breeding population with contributions from an unbalanced family structure of just 10 males and 2 females. Heritability values ranged from 0.54 (±0.21) for body weight to 0.65 (±0.22) for standard body length and were low for cortisol response i.e. 0.08 (±0.06). Genetic correlations were positive (0.94) between standard body length and body weight and negative between cortisol and body weight and between cortisol and standard body length (−0.60 and −0.55, respectively).ConclusionThis study confirms that in European sea bass, heritability of growth-related traits is high and that selection on such traits has potential. However, heritability of cortisol response to stress is low in European sea bass and since it is known to vary greatly among species, further studies are necessary to understand the reasons for these differences.
- SuperSAGE digital expression analysis of differential growth rate in a European sea bass populationPublication . Louro, Bruno; Martins, Rute S.T.; Pinto, Patricia IS; Reinhardt, Richard; de Koning, Dirk-Jan; Canario, Adelino; Power, DeborahOne of the goals of the aquaculture industry is to understand and control growth associated traits through selective breeding. In the present study the molecular basis of growth heterogeneity in the European sea bass (Dicentrarchus labrax) was addressed. To establish growth heterogeneity in a group of hatchery bred sea bass individuals were tagged and their specific growth rates (SGR) determined at monthly intervals. Gene expression in the brain, liver and white muscle from fish with the most divergent sustained SGR (6 individuals of the first and last quartile) was assessed using SuperSAGE (Serial Analysis Gene Expression) combined with next generation SOLiD4 sequencing. A total of approx. 11 million edited tags (26 bp), on average 2 million tags per SAGE library, that represented 47.071 unique transcripts were identified. Comparison of transcripts in fish with high and low SGR yielded 344, 698 and 601 differently expressed tags (0.01% false discovery rate and 4-fold change) in brain, liver and muscle, respectively. The tags were mapped onto the sea bass genome and approximately one third of the tags could be assigned to annotated genes. Pathway enrichment analysis revealed in liver, muscle and brain intricate gene expression changes in endocrine regulatory pathways involved in growth, metabolic and the stress axis, underlying divergent SGR in sea bass.
- An integrated and comparative approach to genetic selection of the aquaculture species Dicentrarchus labraxPublication . Louro, Bruno; Power, DeborahThe European sea bass, Dicentrarchus labrax, is one of the most important marine species cultivated in Southern Europe and has not benefited from selective breeding. One of the major goals in the sea bass (D. labrax) aquaculture industry is to understand and control the complexity of growth associated traits. The aim of the methodology developed for the studies reported in the thesis was not only to establish genetic and genomic resources for sea bass, but to also develop a conceptual strategy to efficiently create knowledge in a research environment that can easily be transferred to the aquaculture industry. The strategy involved; i) establishing an annotated sea bass transcriptome and then using it to, ii) identify new genetic markers for target QTL regions so that, iii) new QTL analysis could be performed and marker based resolution of the DNA regions of interest increased, and then iv) to merge the linkage map and the physical map in order to map the QTL confidence intervals to the sea bass genome and identify genes underlying the targeted traits. Finally to test if genes in the QTL regions that are candidates for divergent growth phenotypes have modified patterns of transcription that reflects the modified whole organism physiology SuperSAGE-SOLiD4 gene expression was used with sea bass with high growth heterogeneity. The SuperSAGE contributed to significantly increase the transcriptome information for sea bass muscle, brain and liver and also led to the identification of putative candidate genes lying in the genomic region of growth related QTL. Lastly all differentially expressed transcripts in brain, liver and muscle of the European sea bass with divergent specific growth rates were mapped to gene pathways and networks and the regulatory pathways most affected identified and established the tissue specific changes underlying the divergent SGR. Owing to the importance of European sea bass to Mediterranean aquaculture and the developed genomics resources from the present thesis and from other studies it should be possible to implement genetic selection programs using marker assisted selection.
- Transcriptomics reveal an integrative role for maternal thyroid hormones during zebrafish embryogenesisPublication . Silva, Nadia; Louro, Bruno; Trindade, Marlene; Power, Deborah M.; Campinho, Marco A.Thyroid hormones (THs) are essential for embryonic brain development but the genetic mechanisms involved in the action of maternal THs (MTHs) are still largely unknown. As the basis for understanding the underlying genetic mechanisms of MTHs regulation we used an established zebrafish monocarboxylic acid transporter 8 (MCT8) knock-down model and characterised the transcriptome in 25hpf zebrafish embryos. Subsequent mapping of differentially expressed genes using Reactome pathway analysis together with in situ expression analysis and immunohistochemistry revealed the genetic networks and cells under MTHs regulation during zebrafish embryogenesis. We found 4,343 differentially expressed genes and the Reactome pathway analysis revealed that TH is involved in 1681 of these pathways. MTHs regulated the expression of core developmental pathways, such as NOTCH and WNT in a cell specific context. The cellular distribution of neural MTH-target genes demonstrated their cell specific action on neural stem cells and differentiated neuron classes. Taken together our data show that MTHs have a role in zebrafish neurogenesis and suggest they may be involved in cross talk between key pathways in neural development. Given that the observed MCT8 zebrafish knockdown phenotype resembles the symptoms in human patients with Allan-Herndon-Dudley syndrome our data open a window into understanding the genetics of this human congenital condition.
- Divergence of duplicate POMC genes in gilthead sea bream Sparus auratusPublication . Cardoso, João; Laiz-Carrión, R.; Louro, Bruno; Silva, Nádia; Canario, Adelino V. M.; Mancera, J. M.; Power, DeborahProopiomelanocorticotrophin (POMC) in vertebrates is produced in the pituitary gland and undergoes post-translational processing to give rise to a range of biologically active peptides. Teleosts possess 2–3 different POMC transcripts which have been proposed to have originated from a whole or partial genome duplication. In the present study 2 transcripts of gilthead sea bream POMC (sbPOMC-a1 and a2) were cloned and characterised. sbPOMC-a1 is expressed principally in the melanotroph cells of the pars intermedia (PI) and sbPOMC-a2 is expressed in the corticotroph cells of the rostral pars distalis and probably also in the PI. The 2 sbPOMC transcripts have a differential tissue distribution in extra-pituitary sites. An appraisal of POMC evolution indicates sbPOMCs belong to one of the two main clades that exist in teleosts and that overall a non conservative process of gene loss occurred in this infraclass.
- CRTAC1 homolog proteins are conserved from cyanobacteria to man and secreted by the teleost fish pituitary glandPublication . Redruello, Begoña; Louro, Bruno; Anjos, Liliana; Silva, Nádia; Greenwell, Roger S.; Canario, Adelino V. M.; Power, DeborahCartilage acidic protein 1 (CRTAC1) gene expression is used as a marker for chondrocyte differentiation instem cell-based tissue engineering. It is also transcribed outside the skeleton where at least two different transcripts are expressed in lung and brain. In the pituitary gland of the teleost fish sea bream Sparus auratus, we have found a transcript with a high degree of sequence identity to CRTAC1 family members but lacking the EGF-like calcium-binding domain encoding sequence of CRTAC1 and designated it as CRTAC2. Database searches revealed many previously unidentified members of the CRTAC1 and CRTAC2 in phylogenetically distant organisms, such as cyanobacteria, bryophyta, lancelets, and diverse representatives of vertebrates. Phylogenetic analyses showed that the genes encoding CRTAC1 and CRTAC2 proteins coexist in teleost fish genomes. Structural prediction analysis identified the N-terminal region of the CRTAC1/CRTAC2 family members as a potential seven-bladed β -propeller structure, closely related to those of integrin α chains and glycosylphosphatidylinositol-specific phospholipase D1 protein families. This relationship is con fi rmed by phylogenetic analysis with the N-terminal domain of sea bream CRTAC2 as the most divergent sequence. Because teleost fi shes are the only phylogenetic group where both CRTAC1 and CRTAC2 genes are present, they occupy a pivotal position in studies of the mechanisms governing the speci fi c expression patterns of each gene/protein subfamily. This will be essential to elucidate their respective biological roles.
- Advances in european sea bass genomics and future perspectivesPublication . Louro, Bruno; Power, Deborah; Canario, Adelino V. M.Only recently available sequenced and annotated teleost fish genomes were restricted to a few model species, none of which were for aquaculture. Application of Marker Assisted Selection for improved production traits had been largely restricted to the salmon industry and genetic and Quantitative Trait Loci (QTL) maps were available for only a few species. With the advent of Next Generatio Sequencing the landscape is rapidly changing and today the genomes of several aquaculture species have been sequenced. The European sea bass, Dicentrarchus labrax, is a good example of a 17 commercially important aquaculture species in Europe for which in the last decade a wealth of genomic resources, including a chromosomal scale genome assembly, physical and linkage maps as well as relevant QTL have been generated. The current challenge is to stimulate the uptake of the resources by the industry so that the full potential of this scientific endeavour can be exploited and produce benefits for producers and the public alike.
- Genomic analysis of Sparus aurata reveals the evolutionary dynamics of sex-biased genes in a sequential hermaphrodite fishPublication . Pauletto, Marianna; Manousaki, Tereza; Ferraresso, Serena; Babbucci, Massimiliano; Tsakogiannis, Alexandros; Louro, Bruno; Vitulo, Nicola; Quoc, Viet Ha; Carraro, Roberta; Bertotto, Daniela; Franch, Rafaella; Maroso, Francesco; Aslam, Muhammad L.; Sonesson, Anna K.; Simionati, Barbara; Malacrida, Giorgio; Cestaro, Alessandro; Caberlotto, Stefano; Sarropoulou, Elena; Mylonas, Costantinos C.; Power, Deborah; Patarnello, Tomaso; Canario, Adelino; Tsigenopoulos, Costas; Bargelloni, LucaSexual dimorphism is a fascinating subject in evolutionary biology and mostly results from sex-biased expression of genes, which have been shown to evolve faster in gonochoristic species. We report here genome and sex-specific transcriptome sequencing of Sparus aurata, a sequential hermaphrodite fish. Evolutionary comparative analysis reveals that sex-biased genes in S. aurata are similar in number and function, but evolved following strikingly divergent patterns compared with gonochoristic species, showing overall slower rates because of stronger functional constraints. Fast evolution is observed only for highly ovary-biased genes due to female-specific patterns of selection that are related to the peculiar reproduction mode of S. aurata, first maturing as male, then as female. To our knowledge, these findings represent the first genome-wide analysis on sex-biased loci in a hermaphrodite vertebrate species, demonstrating how having two sexes in the same individual profoundly affects the fate of a large set of evolutionarily relevant genes.