PIWI-interacting RNAs (piRNA) suppress selfish genetic elements and are essential for germ cell biology in animals. They also play critical roles in regeneration in planaria, regulate gene expression in adult mammalian testes, and participate in antiviral defense in mosquitoes. Inspired by a recent workshop on PIWI proteins and piRNAs, this commentary aims to summarize fundamental aspects of piRNA biology, highlight recent advances, and discuss key outstanding questions. It is written by and for biochemists, geneticists, and evolutionary biologists, and represents our interdisciplinary perspective.

This commentary highlights, from an interdisciplinary perspective, recent advances and key outstanding questions in the field of piRNA biology. [Image: see text]

• Publication type
• Journal Article MeSH

PIWI-interacting RNAs (piRNAs) play a crucial role in safeguarding genome integrity by silencing mobile genetic elements. From flies to humans, piRNAs originate from long single-stranded precursors encoded by genomic piRNA clusters. How piRNA clusters form to adapt to genomic invaders and evolve to maintain protection remain key outstanding questions. Here, we generate a roadmap of piRNA clusters across seven species that highlights both similarities and variations. In mammals, we identify transcriptional readthrough as a mechanism to generate piRNAs from transposon insertions (piCs) downstream of genes (DoG). Together with the well-known stress-dependent DoG transcripts, our findings suggest a molecular mechanism for the formation of piRNA clusters in response to retroviral invasion. Finally, we identify a class of dynamic piRNA clusters in humans, underscoring unique features of human germ cell biology. Our results advance the understanding of conserved principles and species-specific variations in piRNA biology and provide tools for future studies.

• Keywords
• CP: Molecular biology, PIWI, evolution, fertility, germ cell, mobile genetic element, piRNA, readthrough transcription, spermatogenesis, stress, transposon,
• MeSH
• Species Specificity MeSH
• Humans MeSH
• RNA, Small Interfering * metabolism   genetics   MeSH
• Mice MeSH
• Piwi-Interacting RNA MeSH
• Dogs MeSH
• Mammals * genetics   MeSH
• DNA Transposable Elements genetics   MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Mice MeSH
• Dogs MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, N.I.H., Intramural MeSH
• Comparative Study MeSH
• Names of Substances
• RNA, Small Interfering * MeSH
• Piwi-Interacting RNA MeSH
• DNA Transposable Elements MeSH

High-resolution ribosome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscapes of early embryo development at an unprecedented level. We analyzed the transcriptome and the polysome- and non-polysome-bound RNA profiles of bovine oocytes (germinal vesicle and metaphase II stages) and early embryos at the two-cell, eight-cell, morula and blastocyst stages, and revealed four modes of translational selectivity: (1) selective translation of non-abundant mRNAs; (2) active, but modest translation of a selection of highly expressed mRNAs; (3) translationally suppressed abundant to moderately abundant mRNAs; and (4) mRNAs associated specifically with monosomes. A strong translational selection of low-abundance transcripts involved in metabolic pathways and lysosomes was found throughout bovine embryonic development. Notably, genes involved in mitochondrial function were prioritized for translation. We found that translation largely reflected transcription in oocytes and two-cell embryos, but observed a marked shift in the translational control in eight-cell embryos that was associated with the main phase of embryonic genome activation. Subsequently, transcription and translation become more synchronized in morulae and blastocysts. Taken together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

• Keywords
• Bovine, Preimplantation embryo development, Ribosome profiling, Transcription, Translation, Translational selectivity,
• MeSH
• Blastocyst * metabolism   MeSH
• Embryonic Development * genetics   MeSH
• Morula metabolism   MeSH
• Oocytes metabolism   MeSH
• Ribosomes genetics   MeSH
• Cattle MeSH
• Pregnancy MeSH
• Gene Expression Regulation, Developmental MeSH
• Animals MeSH
• Check Tag
• Cattle MeSH
• Pregnancy MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH