Université Côte d'Azur, CNRS, Inserm, IBV, Nice, France.
PLoS One. 2021 Dec 8;16(12):e0260573. doi: 10.1371/journal.pone.0260573. eCollection 2021.
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.
在高度多变且经常充满压力的环境中维持繁殖是所有生物面临的一项基本挑战。即使是短暂暴露于轻度环境应激下，也可能直接损害生殖细胞，或者仅仅对个体的生理机能造成压力，从而使其难以产生优质的配子。在秀丽隐杆线虫中，很大一部分生殖细胞充当营养细胞，在最终经历所谓的生理性生殖细胞凋亡之前，为正在发育的卵母细胞提供支持。尽管对线虫凋亡进行了广泛研究，但对于生态相关环境应激如何影响生殖细胞凋亡知之甚少。此外，生殖细胞凋亡在多大程度上有助于维持卵母细胞质量，进而维持在这种条件下的后代活力，目前仍不清楚。在这里，我们表明，暴露于各种环境应激源（饥饿、乙醇、酸和轻度氧化应激）会增加生殖细胞凋亡，这与先前关于应激诱导凋亡的报告一致。通过使用 ced-3 和 ced-4 的功能丧失突变等位基因，我们证明当母亲在成年早期暴露于这些环境应激源时，消除核心凋亡机制会强烈降低胚胎的存活率。相比之下，ced-9 和 egl-1 的突变主要阻止体细胞中的凋亡，但不阻止生殖细胞中的凋亡，在环境应激下并未表现出这种降低的胚胎存活率。因此，线虫生殖细胞凋亡在维持不良环境中后代的适应性方面发挥着至关重要的作用。最后，我们发现当母亲暴露于环境应激时，ced-3 和 ced-4 突变体的胚胎大小减小并且胚胎形状发生变化。这些观察结果可能表明由于缺乏生殖细胞凋亡，卵母细胞的供应不足。总之，我们的研究结果表明，凋亡途径的核心基因在维持配子质量以及在生态相关环境条件下维持后代适应性方面发挥着关键作用。
