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Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs

Yu H. Sun, Ruoqiao Huiyi Wang, Khai Du, Jiang Zhu, Jihong Zheng, Li Huitong Xie, Amanda A. Pereira, Chao Zhang, Emiliano P. Ricci and Xin Zhiguo Li ()
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Yu H. Sun: University of Rochester Medical Center
Ruoqiao Huiyi Wang: University of Rochester Medical Center
Khai Du: University of Rochester Medical Center
Jiang Zhu: University of Rochester Medical Center
Jihong Zheng: Tongji University
Li Huitong Xie: University of Rochester Medical Center
Amanda A. Pereira: University of Rochester Medical Center
Chao Zhang: Tongji University
Emiliano P. Ricci: Université de Lyon, ENSL, UCBL, INSERM, CNRS, LBMC
Xin Zhiguo Li: University of Rochester Medical Center

Nature Communications, 2021, vol. 12, issue 1, 1-19

Abstract: Abstract PIWI-interacting small RNAs (piRNAs) protect the germline genome and are essential for fertility. piRNAs originate from transposable element (TE) RNAs, long non-coding RNAs, or 3´ untranslated regions (3´UTRs) of protein-coding messenger genes, with the last being the least characterized of the three piRNA classes. Here, we demonstrate that the precursors of 3´UTR piRNAs are full-length mRNAs and that post-termination 80S ribosomes guide piRNA production on 3´UTRs in mice and chickens. At the pachytene stage, when other co-translational RNA surveillance pathways are sequestered, piRNA biogenesis degrades mRNAs right after pioneer rounds of translation and fine-tunes protein production from mRNAs. Although 3´UTR piRNA precursor mRNAs code for distinct proteins in mice and chickens, they all harbor embedded TEs and produce piRNAs that cleave TEs. Altogether, we discover a function of the piRNA pathway in fine-tuning protein production and reveal a conserved piRNA biogenesis mechanism that recognizes translating RNAs in amniotes.

Date: 2021
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DOI: 10.1038/s41467-021-26233-8

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