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Comparative piRNAs Profiles Give a Clue to Transgenerational Inheritance of Sex-Biased piRNAs in Cynoglossus semilaevis

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Abstract

Piwi interacting RNAs (piRNAs) are involved in the epigenetic and post-transcriptional gene silencing of retrotransposons in germ line cells, especially in spermatogenesis. There are many related reports on model organisms, such as flies and mice. In fish, however, there are few studies on piRNAs. Cynoglossus semilaevis, a benthic warm water flatfish, with remarkable sexual dimorphism, especially the “pseudo males” with sex reversal, mating with normal females to produce viable offspring, is an ideal material for the study of sex development. Here, sperm piwi-interacting RNAs profiles of Cynoglossus semilaevis were characterized, comparing between male and pseudomale groups. Differential piRNAs were identified with their predicted and annotated targets. Attention was then focused on candidate piRNAs associated with sex development and methylation. We continued to compare the expression levels of 10 candidates differentially expressed piRNAs in F1 spermatozoa. Quantitative RT-PCR demonstrated that five of the ten piRNAs showed sex bias consistent with parental sequencing results, with four significantly higher expression level in sperm of five males offspring than that of pseudomales, while one piRNAs showed the opposite expression profile. The five signature piRNAs (piR-mmu-49600337, piR-mmu-95849, piR-xtr-7474223, piR-xtr-1790334, and piR-mmu-4491546) could be employed as male-specific molecular biomarkers for C. semilaevis. Besides, this study also implied the possibility of transgenerational inheritance of sex-biased piRNAs exiting in sperm of Cynoglossus semilaevis.

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Funding

This work was supported by grants from the Tianjin Natural Science Foundation (17JCQNJC15000), the Transformation Project of Tianjin Agricultural Achievements (201604090), the Special Funding for Modern Agricultural Industrial Technology System (CARS-47-Z01), and the Funding Project of Southern Marine Science and Engineering Guangdong Laboratory-Zhanjiang 2019 (ZJW-2019–06).

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Authors and Affiliations

  1. Fisheries College, Guangdong Ocean University, 524000, Guangdong, People’s Republic of China

    Na Zhao, Qiuxia Deng, Chunhua Zhu & Bo Zhang

  2. Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, China

    Na Zhao, Qiuxia Deng, Chunhua Zhu & Bo Zhang

  3. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Shanghai Ocean University), Ministry of Education, Shanghai, China

    Na Zhao

  4. International Research Center for Marine Biosciences at, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China

    Na Zhao

  5. Tianjin Fisheries Research Institute, Tianjin, 300201, China

    Lei Jia

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  1. Na Zhao
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  2. Lei Jia
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  3. Qiuxia Deng
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  4. Chunhua Zhu
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  5. Bo Zhang
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Contributions

BZ and CHZ conceived and designed the project. BZ and NZ carried out computational analysis and expression profiling. NZ contributed to the qRT-PCR analysis. NZ wrote the manuscript. JL and QXD edited the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Chunhua Zhu or Bo Zhang.

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Ethics Approval and Consent to Participate

Weizhuo Ltd. (Tangshan, China) provided live C. semilaevis as semen donors for research. The methods for C. semilaevis research were carried out in accordance with the relevant guidelines and regulations. The protocols were approved by the academic ethics committee of Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang.

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Zhao, N., Jia, L., Deng, Q. et al. Comparative piRNAs Profiles Give a Clue to Transgenerational Inheritance of Sex-Biased piRNAs in Cynoglossus semilaevis. Mar Biotechnol 24, 335–344 (2022). https://doi.org/10.1007/s10126-022-10109-z

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