piRNA-guided intron removal from pre-mRNAs regulates density-dependent reproductive strategy

Jing He; Ya Nan Zhu; Bingcai Wang; Pengcheng Yang; Wei Guo; Bo Liang; Feng Jiang; Huimin Wang; Yuanyuan Wei; Le Kang

doi:10.1016/j.celrep.2022.110593

piRNA-guided intron removal from pre-mRNAs regulates density-dependent reproductive strategy

Cell Rep. 2022 Apr 26;39(4):110593. doi: 10.1016/j.celrep.2022.110593.

Authors

Jing He¹, Ya Nan Zhu², Bingcai Wang², Pengcheng Yang³, Wei Guo¹, Bo Liang², Feng Jiang⁴, Huimin Wang³, Yuanyuan Wei⁵, Le Kang⁶

Affiliations

¹ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100101, China.
² State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
³ Beijing Institutes of Life Sciences, Chinese Academy of Sciences, Beijing 100101, China.
⁴ CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100101, China; Beijing Institutes of Life Sciences, Chinese Academy of Sciences, Beijing 100101, China.
⁵ Department of Immunology, Shanghai Key Laboratory of Bioactive Small Molecules and State Key Laboratory of Medical Neurobiology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China. Electronic address: ywei@fudan.edu.cn.
⁶ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100101, China; College of Life Science, Hebei University, Baoding, Hebei 071002, China. Electronic address: lkang@ioz.ac.cn.

PMID: 35476998
DOI: 10.1016/j.celrep.2022.110593

Abstract

Animal density-dependent experiences have profound effects on reproductive strategies with marked fecundity differences. Migratory locust adopts distinct population density-dependent reproductive strategies to cope with their respective life cycles, but the mechanisms remain poorly understood. Here, we report that Piwi-interacting RNAs (piRNAs) in the locust germline play key roles in this process. We find that the locust Piwi protein Liwi1 and piRNAs are highly expressed in early developing egg chambers in solitarious locusts, which have higher fecundity than gregarious locusts. Approximately 40% of solitarious locust-associated piRNAs map to protein-coding genes. We find that Liwi1/piRNAs facilitate pre-mRNA splicing of oocyte development-related genes, such as oo18 RNA-binding protein (Orb), in the germline by recruiting the splicing factor U2AF35 to piRNA-targeted introns, thereby increasing fecundity. Such piRNA-guided pre-mRNA splicing is also functional in Drosophila and mouse germ cells. We uncover a piRNA-guided splicing mechanism for processing reproduction-related mRNAs and determining animal reproductive strategies.

Keywords: CP: Molecular Biology; Orb; Piwi-interacting RNAs; fecundity plasticity; spliceosomes.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Drosophila
Grasshoppers*
Introns / genetics
Mice
RNA Precursors* / genetics
RNA Splicing
RNA, Small Interfering
Reproduction / genetics

Substances

RNA Precursors
RNA, Small Interfering