Gene Expression Changes after Parental Exposure to Metals in the Sea Urchin Affect Timing of Genetic Programme of Embryo Development

Simple Summary Intergenerational and transgenerational effects, in which exposure to stressors in a parental generation affects the phenotype of the offspring have been connected to anthropic impacts on biological systems. Therefore, environmental stress experienced inside a generation, particularly during gametogenesis, may lead to erroneous patterns in their offspring just emerging at early developmental stages. In this scenario, the sea urchin embryo represents a suitable model for integrating analyses of gene expression through embryogenesis with developmental alteration induced by environmental stressors. Herein we provide pieces of evidence for the alteration of the gene regulatory networks modulating embryo development after parental conditioning via non-lethal metal exposure. We show that the parentals' conditioning does not affect viability but significantly impairs the developmental fate of the progeny and regulatory network across a generation. It is reasonable to suppose that changes in Paracentrotus lividus gonads may modify the expression of regulatory genes modulating synthesis and/or accumulation of maternal determinants, which, in turn, impaired the zygotic activation of GRNs responsible for proper embryo development. It is widely accepted that phenotypic traits can be modulated at the epigenetic level so that some conditions can affect the progeny of exposed individuals. To assess if the exposure of adult animals could result in effects on the offspring, the Mediterranean sea urchin and its well-characterized gene regulatory networks (GRNs) was chosen as a model. Adult animals were exposed to known concentrations of zinc and cadmium (both individually and in combination) for 10 days, and the resulting embryos were followed during the development. The oxidative stress occurring in parental gonads, embryo phenotypes and mortality, and the expression level of a set of selected genes, including members of the skeletogenic and endodermal GRNs, were evaluated. Increased oxidative stress at F-0, high rates of developmental aberration with impaired gastrulation, in association to deregulation of genes involved in skeletogenesis (dri, hex, sm50, p16, p19, msp130), endodermal specification (foxa, hox11/13b, wnt8) and epigenetic regulation (kat2A, hdac1, ehmt2, phf8 and UBE2a) occurred either at 24 or 48 hpf. Results strongly indicate that exposure to environmental pollutants can affect not only directly challenged animals but also their progeny (at least F-1), influencing optimal timing of genetic programme of embryo development, resulting in an overall impairment of developmental success.

Automated summary

Exposure to environmental stressors during gametogenesis in parental generation may lead to developmental fate changes and regulatory network alterations in offspring, as demonstrated in sea urchin embryos. Results suggest that exposure to pollutants can impact not only directly exposed animals, but also their progeny, affecting genetic programming and developmental success.