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Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs

View ORCID ProfileYu H. Sun, Ruoqiao Huiyi Wang, Khai Du, Jihong Zheng, Li Huitong Xie, Amanda A. Pereira, Chao Zhang, View ORCID ProfileEmiliano P. Ricci, View ORCID ProfileXin Zhiguo Li
doi: https://doi.org/10.1101/2021.07.10.451906
Yu H. Sun
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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Ruoqiao Huiyi Wang
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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Khai Du
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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Jihong Zheng
2School of Life Sciences and Technology, Tongji University, Shanghai, 200092, China
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Li Huitong Xie
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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Amanda A. Pereira
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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Chao Zhang
2School of Life Sciences and Technology, Tongji University, Shanghai, 200092, China
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Emiliano P. Ricci
3Université de Lyon, ENSL, UCBL, INSERM, CNRS, LBMC, 46 Allée d’Italie, 69007, Lyon, France
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Xin Zhiguo Li
1Center for RNA Biology: From Genome to Therapeutics, Department of Biochemistry and Biophysics, University of Rochester Medical Center, Rochester, NY, 14642, USA
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  • For correspondence: Xin_Li@urmc.rochester.edu
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ABSTRACT

PIWI-interacting small RNAs (piRNAs) protect the germline genome and are essential for fertility. Previously, we showed that ribosomes guide the biogenesis of piRNAs from long non-coding RNAs (lncRNAs) after translating the short open reading frames (ORFs) near their 5′ cap. It remained unclear, however, how ribosomes proceed downstream of ORFs and how piRNA precursors distinguish from other RNAs. It is thus important to test whether a short ORF length is required for substrate recognition for ribosome guided-piRNA biogenesis. Here, we characterized a poorly understood class of piRNAs that originate from the 3′ untranslated regions (3′UTRs) of protein coding genes in mice and chickens. We demonstrate that their precursors are full-length mRNAs and that post-termination 80S ribosomes guide piRNA production on 3′UTRs after translation of upstream long ORFs. Similar to non-sense mediated decay (NMD), piRNA biogenesis degrades mRNA right after pioneer rounds of translation and fine-tunes protein production from mRNAs. Interestingly, however, we found that NMD, along with other surveillance pathways for ribosome recycling are temporally sequestered during the pachytene stage to allow for robust piRNA production. Although 3′UTR piRNA precursor mRNAs code for distinct proteins in mice and chickens, they all harbor embedded transposable elements (TEs) and produce piRNAs that cleave TEs, suggesting that TE suppression, rather than the function of proteins, is the primary evolutionary force maintaining a subset of mRNAs as piRNA precursors. Altogether, we discover a function of the piRNA pathway in fine-tuning protein production and reveal a conserved, general piRNA biogenesis mechanism that recognizes translating RNAs regardless of their ORF length in amniotes.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 11, 2021.
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Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs
Yu H. Sun, Ruoqiao Huiyi Wang, Khai Du, Jihong Zheng, Li Huitong Xie, Amanda A. Pereira, Chao Zhang, Emiliano P. Ricci, Xin Zhiguo Li
bioRxiv 2021.07.10.451906; doi: https://doi.org/10.1101/2021.07.10.451906
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Coupled protein synthesis and ribosome-guided piRNA processing on mRNAs
Yu H. Sun, Ruoqiao Huiyi Wang, Khai Du, Jihong Zheng, Li Huitong Xie, Amanda A. Pereira, Chao Zhang, Emiliano P. Ricci, Xin Zhiguo Li
bioRxiv 2021.07.10.451906; doi: https://doi.org/10.1101/2021.07.10.451906

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