Journal Article

Germ cell apoptosis is critical to maintain Caenorhabditis elegans offspring viability in stressful environments

Braendle, Christian, Fausett, Sarah, Bellone, Michele, Vielle, Anne, Gimond, Clotilde, Poullet, Nausicaa, ANR-17-CE02-0017,ExpEvolGermline,Evolution experimentalle de la ligne germinale de Caenorhabditis elegans en reponse a differents systemes de reproduction, Institut de Biologie Valrose (IBV) ; Université Nice Sophia Antipolis (1965 - 2019) (UNS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Côte d'Azur (UniCA)

2021

Overview

Maintaining reproduction in highly variable, often stressful, environments is an essential challenge for all organisms. Even transient exposure to mild environmental stress may directly damage germ cells or simply tax the physiology of an individual, making it difficult to produce quality gametes. In Caenorhabditis elegans , a large fraction of germ cells acts as nurse cells, supporting developing oocytes before eventually undergoing so-called physiological germ cell apoptosis. Although C . elegans apoptosis has been extensively studied, little is known about how germline apoptosis is influenced by ecologically relevant environmental stress. Moreover, it remains unclear to what extent germline apoptosis contributes to maintaining oocyte quality, and thus offspring viability, in such conditions. Here we show that exposure to diverse environmental stressors, likely occurring in the natural C . elegans habitat (starvation, ethanol, acid, and mild oxidative stress), increases germline apoptosis, consistent with previous reports on stress-induced apoptosis. Using loss-of-function mutant alleles of ced-3 and ced-4 , we demonstrate that eliminating the core apoptotic machinery strongly reduces embryonic survival when mothers are exposed to such environmental stressors during early adult life. In contrast, mutations in ced-9 and egl-1 that primarily block apoptosis in the soma but not in the germline, did not exhibit such reduced embryonic survival under environmental stress. Therefore, C . elegans germ cell apoptosis plays an essential role in maintaining offspring fitness in adverse environments. Finally, we show that ced-3 and ced-4 mutants exhibit concomitant decreases in embryo size and changes in embryo shape when mothers are exposed to environmental stress. These observations may indicate inadequate oocyte provisioning due to the absence of germ cell apoptosis. Taken together, our results show that the central genes of the apoptosis pathway play a key role in maintaining gamete quality, and thus offspring fitness, under ecologically relevant environmental conditions.

• Publisher: CCSD,Public Library of Science,Public Library of Science (PLoS)
• Subject: Animals / Apoptosis / Biology / Biology and Life Sciences / Caenorhabditis elegans / Caenorhabditis elegans - drug effects / Caenorhabditis elegans - growth & development / Caenorhabditis elegans Proteins - genetics / Caspases - genetics / Development Biology / Ecological effects / Embryos / Environmental conditions / Environmental stress / Ethanol / Ethanol - toxicity / Evaluation / Exposure / Female / Fitness / Gametes / Gametocytes / Genetic aspects / Germ cells / Hydrochloric Acid - toxicity / Life Sciences / Male / Membrane Proteins - genetics / Mutants / Mutation / Nematodes / Nurse cells / Offspring / Oocytes / Oocytes - cytology / Oocytes - drug effects / Oocytes - growth & development / Oxidative Stress / Paraquat - toxicity / Physical Sciences / Physiology / Proteins / Proto-Oncogene Proteins c-bcl-2 - genetics / Provisioning / Repressor Proteins - genetics / Reproduction - drug effects / Reproductive fitness / Research and Analysis Methods / Starvation / Stem cells / Stress, Physiological / Survival / Uterus
• ISBN: 0007546252000