mtRBP complex AMG-1/SLRP-1 mediates germline development and spermatogenesis by maintaining mitochondrial homeostasis in Caenorhabditis elegans

Abstract The RNA-binding proteins (RBPs)-mediated post-transcriptional regulation of pre-existing mRNAs is essential for spermatogenesis. But the underlying mechanisms remain poorly understood. Here, we identify a germline-specific mitochondrial RBP AMG-1, a homolog of mammalian LRPPRC, required for spermatogenesis in C. elegans. amg-1 mutation leads to the germline-specific mitochondrial dysfunctions associated with aberrant mitochondrial morphology and structure, which eventually hinders germline development without affecting somatic development. We demonstrate that AMG-1 most frequently binds to mitochondrial DNA-encoded 16S and 12S ribosomal RNAs, the essential components of mitochondrial ribosome, and that 12S rRNA expression mediated by AMG-1 is crucial for germline mitochondrial protein homeostasis. Besides, mitochondrial dysfunction caused by AMG-1 mutation triggers sperm apoptosis in C. elegans. Furthermore, SLRP-1, the homolog of mammalian SLIRP in C. elegans, interacts with AMG-1 genetically to regulate germline development and reproductive success. Taken together, these findings reveal the novel function of a mitochondrial RBP in specifically regulating germline development.