Identification of a complex population of chromatin-associated proteins in the European sea bass (<i>Dicentrarchus labrax</i>) sperm

Barrachina, Ferran; Anastasiadi, Dafni; Jodar, Meritxell; Castillo, Judit; Estanyol, Josep Marı́a; Piferrer, Francesc; Oliva, Rafael

doi:10.1080/19396368.2018.1482383

Cited by 14 publications

(8 citation statements)

References 158 publications

(210 reference statements)

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“…However, they could also be regarded as a sort of 'essential epigenetic marks', as defined elsewhere [37], with respect to dynamic CpGs, which when properly combined can help to predict phenotypic sex (see below). Also, in a recent study in the European sea bass we have shown that the sperm, in addition to its DNA, carries a complex population of chromatin-associated proteins [75], providing further possibilities for the epigenetic transmission of information across generations.…”

Section: Discussionmentioning

confidence: 94%

Dynamic epimarks in sex-related genes predict gonad phenotype in the European sea bass, a fish with mixed genetic and environmental sex determination

et al. 2018

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The integration of genomic and environmental influences into methylation patterns to bring about a phenotype is of central interest in developmental epigenetics, but many details are still unclear. The sex ratios of the species used here, the European sea bass, are determined by genetic and temperature influences. We created four families from parents known to produce offspring with different sex ratios, exposed larvae to masculinizing temperatures and examined, in juvenile gonads, the DNA methylation of seven genes related to sexual development by a targeted sequencing approach. The genes most affected by both genetics and environment were cyp19a1a and dmrt1, with contrasting sex-specific methylation and temperature responses. The relationship between cyp19a1a methylation and expression is relevant to the epigenetic regulation of vertebrate sex, and we report the evidence of such relationship only below a methylation threshold,~80%, and that it was sex-specific: negatively correlated in females but positively correlated in males. From parents to offspring, the methylation in gonads was midway between oocytes and sperm, with bias towards oocytes for amh-r2, er-β2, fsh-r and cyp19a1a. In contrast, dmrt1 levels resembled those of sperm. The methylation of individual CpGs from foxl2, er-β2 and nr3c1 were conserved from parents to offspring, whereas those of cyp19a1a, dmrt1 and amh-r2 were affected by temperature. Utilizing a machine-learning procedure based on the methylation levels of a selected set of CpGs, we present the first, to our knowledge, system based on epigenetic marks capable of predicting sex in an animal with~90% accuracy and discuss possible applications.

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Section: Discussionmentioning

confidence: 94%

Dynamic epimarks in sex-related genes predict gonad phenotype in the European sea bass, a fish with mixed genetic and environmental sex determination

et al. 2018

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“…The European sea bass has become one of the most studied species in sh epigenetics [77][78][79][80][81][82][83][84]. Because of the availability of its genome and the development of selection programs, efforts should be dedicated to further explore its epigenomic landscape regarding the stress response, especially in an aquaculture context.…”

Section: Resultsmentioning

confidence: 99%

“…It has been extensively studied over the last three decades, for both natural and farmed populations (reviewed in [75]). This includes the sequencing of its genome [76] and an increasing number of epigenetic studies [77][78][79][80][81][82][83][84]. The stress response of European sea bass remains evaluated using blood parameters that have been shown to re ect multiple components of its stress response [16,85], despite authors have proposed alternatives [86,87].…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Epigenomic Stress Response in the European Sea Bass (Dicentrarchus Labrax, L.)

Krick

DESMARAIS

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et al. 2020

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Background: While the stress response inspired genome-wide epigenetic studies in vertebrate models, it remains mostly ignored in fish. We modified the epiGBS (epiGenotyping By sequencing) technique to explore changes in genome-wide cytosine methylation to a repeated acute stress challenge in the nucleated red blood cells (RBCs) of the European sea bass (Dicentrarchus labrax). This species is widely studied in both the natural and farmed environments, including issues regarding health and welfare.Results: We retrieved 501,108,033 sequencing reads after trimming, with a mean mapping efficiency of 73.0% (unique best hits). Fifty-seven differentially methylated cytosines (DMCs) close to 51 distinct stress-related genes distributed on 17 of 24 linkage groups (LGs) were detected between RBCs of pre- and post-stress individuals. Literature surveys indicated that thirty-eight of these genes were previously reported as differentially expressed in the brain of zebrafish, most of them involved in stress coping differences. DMC-related genes associated to the Brain Derived Neurotrophic Factor, a protein that favors stress adaptation and fear memory, are especially relevant.Conclusion: We provide an improved epiGBS protocol with increased multiplexing and sequencing capacities that offer new opportunities to improve data acquisition and to investigate important biological processes at a genome-wide level, such as the stress response. Minimally invasive RBCs deserve more attention to investigate the epigenetic response to stress without sacrificing fish.

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“…Several collaborative projects were developed and published with Gordon in subsequent years after Rafael had completed his postdoctoral training and become established as an independent scientist at the University of Barcelona (54,55). The appreciation for the reproductive biology experimental model from Gordon, as a major mentor, determined the primary focus of Rafael's subsequent scientific career, with a substantial imprint in the study of the protamines, chromatin structure and the 'omic' composition in spermatogenesis (de Yebra et al 1993;Oliva 2006;Jodar et al 2011;Castillo et al 2014Castillo et al , 2018Barrachina et al 2018;Soler-Ventura et al 2019).…”

Section: The University Of Calgary (1974-1994)mentioning

confidence: 99%

Gordon Henry Dixon. 25 March 1930—24 July 2016

Oliva

Krawetz

2020

Biogr. Mems Fell. R. Soc.

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Gordon H. Dixon was a highly influential scientist who excelled in all the stages of his career and in each laboratory of every institution at which he was a member. Gordon began his graduate career at the University of Cambridge and completed his studies at the University of Toronto on the subject of transpeptidation reactions in biological systems. At an early stage of his career, he developed the technique of starch gel electrophoresis with Oliver Smithies and made important discoveries on the structure of human haptoglobins. Subsequently, Gordon contributed to the determination of the structure and active sites and mechanisms of action of trypsin and chymotrypsin and made seminal discoveries related to understanding the structure of the protein hormone insulin. However, he is best known for his later studies on the regulation of protamine genes and chromatin transitions in spermatogenesis. He is often considered to be the father of the protamine molecular biology underlying this gene system and his research is continually cited to this day. Gordon contributed to the identification and sequencing of the protamine genes, the discovery that methionine was required for initiation of protamine synthesis, understanding the roles of histone hyperacetylation and protamine phosphorylation, and the generation of the highly compact nucleoprotamine structure present in sperm, primarily using trout as a model system. Gordon is fondly remembered as a brilliant and very generous scientist by all his mentees, representing all levels from undergraduates to PhD and postdoctoral fellows, who provided a scientifically stimulating atmosphere in which they could develop their careers. From a more personal perspective, he also had a fun side and was devoted to his family. Gordon was a person who, owing to his legacy of great science and his fundamental humanity, still lives in the memory of many people.

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Identification of a complex population of chromatin-associated proteins in the European sea bass (Dicentrarchus labrax) sperm

Cited by 14 publications

References 158 publications

Dynamic epimarks in sex-related genes predict gonad phenotype in the European sea bass, a fish with mixed genetic and environmental sex determination

Dynamic epimarks in sex-related genes predict gonad phenotype in the European sea bass, a fish with mixed genetic and environmental sex determination

Genome-Wide Epigenomic Stress Response in the European Sea Bass (Dicentrarchus Labrax, L.)

Gordon Henry Dixon. 25 March 1930—24 July 2016

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