Parental exposure to environmental concentrations of diuron leads to aneuploidy in embryos of the Pacific oyster, as evidenced by fluorescent in situ hybridization

Barranger, Audrey; Benabdelmouna, Abdellah; Dégremont, Lionel; Burgeot, Thierry; Akcha, Farida

doi:10.1016/j.aquatox.2014.11.011

Cited by 19 publications

(14 citation statements)

References 56 publications

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“…Genotoxicity on gamete and somatic cells (Bouilly et al 2007;Akcha et al 2012;Barranger et al 2014), embryotoxicity (Akcha et al 2012;Barranger et al 2014) and immunotoxicity (Gagnaire et al 2007;Luna-Acosta et al 2012;Barranger et al 2015) were already reported after exposure to 0.05 to 3.00 μg.L -1 of diuron depending on the studies. As already demonstrated for other herbicides such as paraquat, glyphosate and atrazine, ROS production could also be involved in the toxicity of diuron (Glusczak et al 2006;Awadalla 2012;Blahová et al 2013;Griboff et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Comparative embryotoxicity and genotoxicity of the herbicide diuron and its metabolites in early life stages of Crassostrea gigas: Implication of reactive oxygen species production

et al. 2016

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Herbicides are one of the major classes of pollutants contaminating coastal waters over the world. Among them, diuron (3-(3,4-dichlorophenyl)-1,1-dimethylurea) is a phenylurea herbicide frequently detected in oyster-producing area, known to be toxic for this important exploited non-target species. With the aim to investigate the mechanisms by which diuron displays its toxicity in oyster, the implication of both biotransformation and oxygen reactive species (ROS) production was studied considering embryotoxicity and genotoxicity as endpoints. Comparative embryotoxicity and genotoxicity of diuron and its main metabolites (DCPMU, DCPU and 3,4-DCA) were thus studied on oyster larvae by the embryo-larval bioassay on D larvae and the comet assay on trochophore larvae, respectively. Exposures were also performed in presence and absence of known ROS scavenger compounds - ascorbic acid and N-acetylcysteine, to evaluate the involvement of oxyradicals in the toxic responses. In the case of diuron, the production of ROS on exposed oyster larvae was also measured using 2',7'-dichlorodihydrofluorescein diacetate as a probe for flow cytometric analysis. The results we obtained showed the embryotoxicity and genotoxicity of diuron and its metabolites in early life stages of the Pacific oyster. For concentrations ranging from 0.05 to 0.5μgL(-1), diuron appeared significantly more embryotoxic than DCPMU and DCPU (p<0.001). Embryotoxicity decreased with diuron metabolism as follows: diuron≥DCPMU=DCPU, highlighting that biotransformation can constitute a true detoxication pathways in oyster larvae by decreasing the toxicity of the parent compound. In the opposite, no difference was observed between diuron and its metabolites concerning larval development when considering a lower and more environmentally realistic range of concentrations (0.002-0.050μgL(-1)). 3,4-DCA was the only compound that did not show any sign of embryotoxicity, even at concentrations up to 5μgL(-1). Concerning genotoxicity, no significant difference was observed between diuron and all of its metabolites including 3, 4 DCA with damages detected from the concentration of 0.05μgL(-1). As for diuron, the toxicity of the metabolites seems to be mediated in some part by ROS production as clearly demonstrated by the decrease in genotoxicity and developmental abnormalities in the presence of the oxidant scavenger, ascorbic acid.

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Section: Introductionmentioning

confidence: 99%

Comparative embryotoxicity and genotoxicity of the herbicide diuron and its metabolites in early life stages of Crassostrea gigas: Implication of reactive oxygen species production

et al. 2016

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“…Some results were previously obtained demonstrating both direct and indirect effects of the parental herbicide exposure on oyster genome. A genotoxic effect has been detected through the evidence of primary DNA damages in both somatic, germinal and reproductive cells of diuron-exposed genitors [ 37 , 38 ]. Moreover, the vertical transmission of damaged DNA was confirmed by the detection of chromosomal abnormalities in the offspring (DNA aneuploidy) [ 38 ].…”

Section: Introductionmentioning

confidence: 99%

“…A genotoxic effect has been detected through the evidence of primary DNA damages in both somatic, germinal and reproductive cells of diuron-exposed genitors [ 37 , 38 ]. Moreover, the vertical transmission of damaged DNA was confirmed by the detection of chromosomal abnormalities in the offspring (DNA aneuploidy) [ 38 ]. By a transcriptional approach, we showed that exposure of oyster genitors to diuron at environmental concentrations affected gene expression including genes encoding enzymes involved in DNA methylation machinery [ 39 ].…”

Section: Introductionmentioning

confidence: 99%

“…By a transcriptional approach, we showed that exposure of oyster genitors to diuron at environmental concentrations affected gene expression including genes encoding enzymes involved in DNA methylation machinery [ 39 ]. In the offspring, a RNA-seq analysis demonstrated significant change in the transcriptional profile on F1 spat as well [ 40 ] that could explain developmental and growth impairment observed in F1 early life stages [ 37 , 38 ].…”

Section: Introductionmentioning

confidence: 99%

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Effects of a parental exposure to diuron on Pacific oyster spat methylome

Rondon¹,

Grunau²,

Fallet³

et al. 2017

Environmental Epigenetics

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Environmental epigenetic is an emerging field that studies the cause–effect relationship between environmental factors and heritable trait via an alteration in epigenetic marks. This field has received much attentions since the impact of environmental factors on different epigenetic marks have been shown to be associated with a broad range of phenotypic disorders in natural ecosystems. Chemical pollutants have been shown to affect immediate epigenetic information carriers of several aquatic species but the heritability of the chromatin marks and the consequences for long term adaptation remain open questions. In this work, we investigated the impact of the diuron herbicide on the DNA methylation pattern of spat from exposed Crassotrea gigas genitors. This oyster is one of the most important mollusk species produced worldwide and a key coastal economic resource in France. The whole genome bisulfite sequencing (WGBS, BS-Seq) was applied to obtain a methylome at single nucleotide resolution on DNA extracted from spat issued from diuron exposed genitors comparatively to control spat. We showed that the parental diuron exposure has an impact on the DNA methylation pattern of its progeny. Most of the differentially methylated regions occurred within coding sequences and we showed that this change in methylation level correlates with RNA level only in a very small group of genes. Although the DNA methylation profile is variable between individuals, we showed conserved DNA methylation patterns in response to parental diuron exposure. This relevant result opens perspectives for the setting of new markers based on epimutations as early indicators of marine pollutions.

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“…Agrochemical inputs are known to display seasonal variations: in France, high pesticide concentrations have been detected in spring in a major shellfish farming zone, the Marennes Oleron basin, corresponding to the highly-sensitive oyster gametogenesis period (Burgeot et al, 2008;Munaron, 2004;Soletchnik et al, 2005). Pesticides not only have direct toxic effects on adult oysters, but also indirect trans-generational effects on their offspring (Barranger et al, 2015(Barranger et al, , 2014Bouilly et al, 2007Bouilly et al, , 2003. In a previous experiment conducted by our laboratory, oyster genitors in gametogenesis were subjected to short exposures (two 7-day pulses) of environmental concentrations of the herbicide diuron (0.3 µg.L −1 ).…”

Section: Introductionmentioning

confidence: 99%

Parental exposure to the herbicide diuron results in oxidative DNA damage to germinal cells of the Pacific oyster Crassostrea gigas

Barranger

Heude-Berthelin

Rouxel

et al. 2016

Comparative Biochemistry and Physiology Part C: Toxicology &

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Chemical pollution by pesticides has been identified as a possible contributing factor to the massive mortality outbreaks observed in Crassostrea gigas for several years. A previous study demonstrated the vertical transmission of DNA damage by subjecting oyster genitors to the herbicide diuron at environmental concentrations during gametogenesis. This trans-generational effect occurs through damage to genitor-exposed gametes, as measured by the comet-assay. The presence of DNA damage in gametes could be linked to the formation of DNA damage in other germ cells. In order to explore this question, the levels and cell distribution of the oxidized base lesion 8-oxodGuo were studied in the gonads of exposed genitors. High-performance liquid chromatography coupled with UV and electrochemical detection analysis showed an increase in 8-oxodGuo levels in both male and female gonads after exposure to diuron. Immunohistochemistry analysis showed the presence of 8-oxodGuo at all stages of male germ cells, from early to mature stages. Conversely, the oxidized base was only present in early germ cell stages in female gonads. These results indicate that male and female genitors underwent oxidative stress following exposure to diuron, resulting in DNA oxidation in both early germ cells and gametes, such as spermatozoa, which could explain the transmission of diuron-induced DNA damage to offspring. Furthermore, immunostaining of early germ cells seems indicates that damages caused by exposure to diuron on germ line not only affect the current sexual cycle but also could affect future gametogenesis.

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Parental exposure to environmental concentrations of diuron leads to aneuploidy in embryos of the Pacific oyster, as evidenced by fluorescent in situ hybridization

Cited by 19 publications

References 56 publications

Comparative embryotoxicity and genotoxicity of the herbicide diuron and its metabolites in early life stages of Crassostrea gigas: Implication of reactive oxygen species production

Comparative embryotoxicity and genotoxicity of the herbicide diuron and its metabolites in early life stages of Crassostrea gigas: Implication of reactive oxygen species production

Effects of a parental exposure to diuron on Pacific oyster spat methylome

Parental exposure to the herbicide diuron results in oxidative DNA damage to germinal cells of the Pacific oyster Crassostrea gigas

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