Local coordination of mRNA storage and degradation near mitochondria modulates C. elegans ageing.

Mitochondria are central regulators of healthspan and lifespan, yet the intricate choreography of multiple, tightly controlled steps regulating mitochondrial biogenesis remains poorly understood. Here, we uncover a pivotal role for specific elements of the 5′‐3′ mRNA degradation pathway in the regulation of mitochondrial abundance and function. We find that the mRNA degradation and the poly‐A tail deadenylase CCR4‐NOT complexes form distinct foci in somatic Caenorhabditis elegans cells that physically and functionally associate with mitochondria. Components of these two multi‐subunit complexes bind transcripts of nuclear‐encoded mitochondria‐targeted proteins to regulate mitochondrial biogenesis during ageing in an opposite manner. In addition, we show that balanced degradation and storage of mitochondria‐targeted protein mRNAs are critical for mitochondrial homeostasis, stress resistance and longevity. Our findings reveal a multifaceted role of mRNA metabolism in mitochondrial biogenesis and show that fine‐tuning of mRNA turnover and local translation control mitochondrial abundance and promote longevity in response to stress and during ageing. Synopsis: Preservation of healthy and functional mitochondria is essential for cellular and organismal homeostasis. This study shows key factors of the mRNA metabolism pathway function in the vicinity of mitochondria to modulate mitochondrial content and consequently, ageing in worms.mRNA degradation and poly‐A tail deadenylase CCR4‐NOT complex form discrete foci at the mitochondrial vicinity.mRNA degradation and storage bodies oppositely regulate mitochondrial biogenesis and abundance.Storage and degradation bodies co‐regulate the fate of nuclear‐encoded, mitochondria‐targeted protein transcripts (MTPTs) near mitochondria.Balanced mRNA storage and degradation is crucial for C. elegans stress resistance and longevity. [ABSTRACT FROM AUTHOR]