Research Article: Apoptosis contributes to protect germ cells from the oogenic germline starvation response but is not essential for the gonad shrinking or recovery observed during adult reproductive diapause in C. elegans

Date Published: June 13, 2019

Publisher: Public Library of Science

Author(s): E. Carranza-García, R. E. Navarro, Myon-Hee Lee.


When C. elegans hermaphrodites are deprived of food during the mid-L4 larval stage and throughout adulthood, they enter an alternative stage termed “adult reproductive diapause (ARD)” in which they halt reproduction and extend their lifespan. During ARD, germ cell proliferation stops; oogenesis is slowed; and the gonad shrinks progressively, which has been described as the “oogenic germline starvation response”. Upon refeeding, the shrunken gonad is regenerated, and animals recover fertility and live out their remaining lifespan. Little is known about the effects of ARD on oocyte quality after ARD. Thus, the aim of this study was to determine how oocyte quality is affected after ARD by measuring brood size and embryonic lethality as a reflection of defective oocyte production. We found that ARD affects reproductive capacity. The oogenic germline starvation response protects oogenic germ cells by slowing oogenesis to prevent prolonged arrest in diakinesis. In contrast to a previous report, we found that germ cell apoptosis is not the cause of gonad shrinkage; instead, we propose that ovulation contributes to gonad shrinkage during the oogenic germline starvation response. We show that germ cell apoptosis increases and continues during ARD via lin-35/Rb and an unknown mechanism. Although apoptosis contributes to maintain germ cell quality during ARD, we demonstrated that apoptosis is not essential to preserve animal fertility. Finally, we show that IIS signaling inactivation partially participates in the oogenic germline starvation response.

Partial Text

To ensure species continuity, animals have developed mechanisms for protecting germ cells during stressful conditions. The C. elegans hermaphrodite germline serves as an excellent model for studying cell biology. In C. elegans hermaphrodites, 2 identical U-shaped gonad arms contain germ cells (Fig 1A). Under control conditions, L4 hermaphrodites (Fig 1C and 1E) produce approximately 40 germ cells that give rise 160 spermatids per gonad arm, which are stored within each spermatheca. Thereafter, during the adult stage, the remaining germ cells either differentiate into oocytes or are eliminated by physiological germline apoptosis [1, 2]. Physiological apoptosis is an essential mechanism for maintaining oocyte quality during oogenesis, as it promotes the allocation of nutrients to growing oocytes [3]. The most proximal oocytes arrest in diakinesis until they are fertilized, then complete meiosis and begin embryogenesis [3, 4] (Fig 1A and 1D). During its fertile period, a hermaphrodite produces approximately 300 new organisms in 3 days by self-fertilization with very low embryonic lethality (approx. 1–2 dead embryos/animal). Then, they cease laying eggs and live for 15 more days [4].

Angelo and van Gilst (2009) reported a novel type of adult reproductive diapause for the first time while studying reproduction when nutrients are limited. They showed that crowded populations of mid-L4 larval stage animals subjected to starvation delay their reproductive cycle and are able to live for up to 30 days without food. Furthermore, when conditions are restored, these animals resume their reproductive cycle and live out a normal lifespan. During ARD, the gonad experiences reversible germ cell loss and size reduction; when animals are returned to food, the gonad regenerates in terms of both germ cell number and size [7].




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