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RESEARCH ARTICLE
PLP-1 is essential for germ cell development and germline gene silencing in Caenorhabditis elegans
Rajaram Vishnupriya, Linitha Thomas, Lamia Wahba, Andrew Fire, Kuppuswamy Subramaniam
Development 2020 147: dev195578 doi: 10.1242/dev.195578 Published 27 November 2020
Rajaram Vishnupriya
1Department of Biotechnology, Indian Institute of Technology–Madras, Chennai 600036, India
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Linitha Thomas
2Department of Biological Sciences & Bioengineering, Indian Institute of Technology, Kanpur 208016, India
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  • ORCID record for Linitha Thomas
Lamia Wahba
3Department of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA
4Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
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Andrew Fire
3Department of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA
4Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA
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Kuppuswamy Subramaniam
1Department of Biotechnology, Indian Institute of Technology–Madras, Chennai 600036, India
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  • ORCID record for Kuppuswamy Subramaniam
  • For correspondence: subbu@iitm.ac.in

Handling Editor: Swathi Arur

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ABSTRACT

The germline genome is guarded against invading foreign genetic elements by small RNA-dependent gene-silencing pathways. Components of these pathways localize to, or form distinct aggregates in the vicinity of, germ granules. These components and their dynamics in and out of granules are currently being intensively studied. Here, we report the identification of PLP-1, a Caenorhabditis elegans protein related to the human single-stranded nucleic acid-binding protein Pur-alpha, as a component of germ granules in C. elegans. We show that PLP-1 is essential for silencing different types of transgenes in the germ line and for suppressing the expression of several endogenous genes controlled by the germline gene-silencing pathways. Our results reveal that PLP-1 functions downstream of small RNA biogenesis during initiation of gene silencing. Based on these results and the earlier findings that Pur-alpha proteins interact with both RNA and protein, we propose that PLP-1 couples certain RNAs with their protein partners in the silencing complex. PLP-1 orthologs localized on RNA granules may similarly contribute to germline gene silencing in other organisms.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: R.V., L.T., K.S.; Methodology: R.V., L.T., L.W., A.F., K.S.; Validation: R.V., L.T., L.W., A.F., K.S.; Formal analysis: R.V., L.T., L.W., A.F., K.S.; Investigation: R.V., L.T., L.W., A.F., K.S.; Resources: A.F., K.S.; Writing - original draft: R.V., L.T., K.S.; Writing - review & editing: K.S.; Supervision: K.S.; Project administration: K.S.; Funding acquisition: K.S.

  • Funding

    Research in the K.S. laboratory is supported by grants from the Department of Biotechnology, Ministry of Science and Technology, India (BT/PR29010/BRB/10/1694/2018) and the Science and Engineering Research Board, Department of Science and Technology, Ministry of Science and Technology, India (EMR/2016/002272). Work in the Fire laboratory is supported by National Institutes of Health grant R35GM130366. Deposited in PMC for release after 12 months.

  • Data availability

    All raw small RNA and mRNA high-throughput sequencing data, and lists of identified C. elegans genes and read counts have been deposited in GEO under accession number GSE161011.

  • Supplementary information

    Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.195578.supplemental

  • Received July 31, 2020.
  • Accepted October 6, 2020.
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Keywords

  • Pur-alpha
  • puf-8
  • P granules
  • piRNA
  • Major sperm proteins

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RESEARCH ARTICLE
PLP-1 is essential for germ cell development and germline gene silencing in Caenorhabditis elegans
Rajaram Vishnupriya, Linitha Thomas, Lamia Wahba, Andrew Fire, Kuppuswamy Subramaniam
Development 2020 147: dev195578 doi: 10.1242/dev.195578 Published 27 November 2020
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RESEARCH ARTICLE
PLP-1 is essential for germ cell development and germline gene silencing in Caenorhabditis elegans
Rajaram Vishnupriya, Linitha Thomas, Lamia Wahba, Andrew Fire, Kuppuswamy Subramaniam
Development 2020 147: dev195578 doi: 10.1242/dev.195578 Published 27 November 2020

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