Meiotic dysfunction accelerates somatic aging in Caenorhabditis elegans

An expanding body of evidence, from studies in model organisms to human clinical data, reveals that reproductive health influences organismal aging. However, the impact of germline integrity on somatic aging is poorly understood. Moreover, assessing the causal relationship of such an impact is challenging to address in human and vertebrate models. Here, we demonstrate that disruption of meiosis, a germline restricted process, shortened lifespan, impaired individual aspects of healthspan, and accelerated somatic aging in Caenorhabditis elegans. Young meiotic mutants exhibited transcriptional profiles that showed remarkable overlap with the transcriptomes of old worms and shared similarities with transcriptomes of aging human tissues as well. We found that meiosis dysfunction caused increased expression of functionally relevant longevity determinants whose inactivation enhanced the lifespan of normal animals. Further, meiotic mutants manifested destabilized protein homeostasis and enhanced proteasomal activity partially rescued the associated lifespan defects. Our study demonstrates a role for meiotic integrity in controlling somatic aging and reveals proteostasis control as a potential mechanism through which germline status impacts overall organismal health.

Automated summary

Reproductive health impacts organismal aging, but the effect of germline integrity on somatic aging is poorly understood. This study shows that disruption of meiosis, a germline restricted process, accelerates somatic aging in Caenorhabditis elegans. Mutants with meiosis dysfunction exhibit transcriptional profiles similar to old worms and aging human tissues. The study also reveals that inactivation of longevity determinants increased the lifespan of normal animals.