Reduced pachytene pi RNAs and translation underlie spermiogenic arrest in Maelstrom mutant mice.

Pachytene pi RNAs are a class of Piwi-interacting small RNAs abundant in spermatids of the adult mouse testis. They are processed from pi RNA primary transcripts by a poorly understood mechanism and, unlike fetal transposon-derived pi RNAs, lack complementary targets in the spermatid transcriptome. We report that immunopurified complexes of a conserved pi RNA pathway protein Maelstrom ( MAEL) are enriched in MIWI (Piwi partner of pachytene piRNAs), Tudor-domain proteins and processing intermediates of pachytene pi RNA primary transcripts. We provide evidence of functional significance of these complexes in Mael 129 knockout mice that exhibit spermiogenic arrest with acrosome and flagellum malformation. Mael 129-null mutant testes possess low levels of pi RNAs derived from MAEL-associated piRNA precursors and exhibit reduced translation of numerous spermiogenic mRNAs including those encoding acrosome and flagellum proteins. These translation defects in haploid round spermatids are likely indirect, as neither MAEL nor pi RNA precursors associate with polyribosomes, and they may arise from an imbalance between pachytene pi RNAs and MIWI. [ABSTRACT FROM AUTHOR]