Bacterial contribution to genesis of the novel germ line determinant oskar

  1. Leo Blondel
  2. Tamsin E M Jones
  3. Cassandra G Extavour  Is a corresponding author
  1. Harvard University, United States
  2. European Bioinformatics Institute, United Kingdom

Abstract

New cellular functions and developmental processes can evolve by modifying existing genes or creating novel genes. Novel genes can arise not only via duplication or mutation but also by acquiring foreign DNA, also called horizontal gene transfer (HGT). Here we show that HGT likely contributed to the creation of a novel gene indispensable for reproduction in some insects. Long considered a novel gene with unknown origin, oskar has evolved to fulfil a crucial role in insect germ cell formation. Our analysis of over 100 insect Oskar sequences suggests that Oskar arose de novo via fusion of eukaryotic and prokaryotic sequences. This work shows that highly unusual gene origin processes can give rise to novel genes that can facilitate evolution of novel developmental mechanisms.

Data availability

All data are available in the main text or the supplementary materials.

Article and author information

Author details

  1. Leo Blondel

    Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2276-4821
  2. Tamsin E M Jones

    HGNC, European Bioinformatics Institute, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0027-0858
  3. Cassandra G Extavour

    Department of Organismic and Evolutionary Biology/Molecular and Cellular Biology, Harvard University, Cambridge, United States
    For correspondence
    extavour@oeb.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2922-5855

Funding

Harvard University

  • Leo Blondel

Harvard University

  • Cassandra G Extavour

Harvard University

  • Tamsin E M Jones

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Publication history

  1. Received: January 29, 2019
  2. Accepted: February 23, 2020
  3. Accepted Manuscript published: February 24, 2020 (version 1)
  4. Version of Record published: May 26, 2020 (version 2)

Copyright

© 2020, Blondel et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,079
    Page views
  • 442
    Downloads
  • 12
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Leo Blondel
  2. Tamsin E M Jones
  3. Cassandra G Extavour
(2020)
Bacterial contribution to genesis of the novel germ line determinant oskar
eLife 9:e45539.
https://doi.org/10.7554/eLife.45539
  1. Further reading

Further reading

    1. Developmental Biology
    Bavat Bornstein, Lia Heinemann-Yerushalmi ... Elazar Zelzer
    Tools and Resources

    The proprioceptive system is essential for the control of coordinated movement, posture and skeletal integrity. The sense of proprioception is produced in the brain using peripheral sensory input from receptors such as the muscle spindle, which detects changes in the length of skeletal muscles. Despite its importance, the molecular composition of the muscle spindle is largely unknown. In this study, we generated comprehensive transcriptomic and proteomic datasets of the entire muscle spindle isolated from the murine deep masseter muscle. We then associated differentially expressed genes with the various tissues composing the spindle using bioinformatic analysis. Immunostaining verified these predictions, thus establishing new markers for the different spindle tissues. Utilizing these markers, we identified the differentiation stages the spindle capsule cells undergo during development. Together, these findings provide comprehensive molecular characterization of the intact spindle as well as new tools to study its development and function in health and disease.

    1. Cancer Biology
    2. Developmental Biology
    Deepti Prasad, Katharina Illek ... Anne-Kathrin Classen
    Research Article

    Tissue-intrinsic defense mechanisms eliminate aberrant cells from epithelia and thereby maintain the health of developing tissues or adult organisms. 'Interface surveillance' comprises one such distinct mechanism that specifically guards against aberrant cells which undergo inappropriate cell fate and differentiation programs. The cellular mechanisms which facilitate detection and elimination of these aberrant cells are currently unknown. We find that in Drosophila imaginal discs, clones of cells with inappropriate activation of cell fate programs induce bilateral JNK activation at clonal interfaces, where wild type and aberrant cells make contact. JNK-activation is required to drive apoptotic elimination of interface cells. Importantly, JNK-activity and apoptosis are highest in interface cells within small aberrant clones, which likely supports the successful elimination of aberrant cells when they arise. Our findings are consitent with a model where clone size affects the topology of interface contacts and thereby the strength of JNK activation in wild type and aberrant interface cells. Bilateral JNK activation is unique to 'interface surveillance' and is not observed in other tissue-intrinsic defense mechanisms, such as classical 'cell-cell competition'. Thus, bilateral JNK interface signaling provides an independent tissue-level mechanism to eliminate cells with inappropriate developmental fate but normal cellular fitness. Finally, oncogenic Ras-expressing clones activate 'interface surveillance' but evade elimination by bilateral JNK activation. Combined, our work establishes bilateral JNK interface signaling and interface apoptosis as a new hallmark of interface surveillance, and highlights how oncogenic mutations evade tumor suppressor function encoded by this tissue-intrinsic surveillance system.