Two distinct mechanisms lead to either oocyte or spermatocyte decrease in C. elegans after whole developmental exposure to γ-rays

ABSTRACT Wildlife is subject to various sources of pollution, including ionizing radiation. Adverse effects can impact organisms’ survival, growth, or reproduction, later affecting population dynamics. In invertebrates, reproduction, which directly impacts population dynamics, has been found to be the most radiosensitive endpoint. Understanding the underlying molecular pathways inducing this reproduction decrease can help to comprehend species-specific differences in radiosensitivity. In line with previous studies, we used a life stage dependent approach to better understand the molecular determinants of reproduction decrease, especially of gamete decrease, in the hermaphrodite roundworm Caenorhabditis elegans. Worms were chronically exposed to 50 mGy·h?1 external gamma ionizing radiations throughout different developmental periods (namely embryogenesis, gametogenesis, and full development). Conserved molecular pathways across invertebrates and vertebrates involved in reproduction processes and stress response were analyzed: apoptosis and MAP kinase Ras/ERK (MPK-1). Our results showed that these pathways are life-stage dependant, resulting from an accumulation of damages upon chronic exposure to IR throughout the whole development. The Ras/ERK pathway was found to be activated in our conditions in the pachytene region of the gonad where it induces the apoptotic pathway, but not in the ovulation zone, showing no incidence on oocyte maturation and ovulation. Additionally, no effect on germ cell proliferation was found, meaning that Ras/ERK pathway is probably not involved in this process in our conditions. Finally, a functional analysis of apoptosis revealed that the decrease of ovulation rate is due to DNA-damaged induced apoptosis which does not occur in spermatocytes. Thus, sperm decrease seem to be mediated via another mechanism, probably a decrease in germ cells proliferation speed that needs further investigation to better characterize sex-specific responses to IR exposure.