A single-cell survey of Drosophila blood

  1. Sudhir Gopal Tattikota  Is a corresponding author
  2. Bumsik Cho
  3. Yifang Liu
  4. Yanhui Hu
  5. Victor Barrera
  6. Michael J Steinbaugh
  7. Sang-Ho Yoon
  8. Aram Comjean
  9. Fangge Li
  10. Franz Dervis
  11. Ruei-Jiun Hung
  12. Jin-Wu Nam
  13. Shannan Ho Sui
  14. Jiwon Shim
  15. Norbert Perrimon  Is a corresponding author
  1. Blavatnik Institute, Harvard Medical School, United States
  2. Hanyang University, Republic of Korea
  3. Harvard T H Chan Bioinformatics Core, United States

Abstract

Drosophila blood cells, called hemocytes, are classified into plasmatocytes, crystal cells, and lamellocytes based on the expression of a few marker genes and cell morphologies, which are inadequate to classify the complete hemocyte repertoire. Here, we used single-cell RNA sequencing (scRNA-seq) to map hemocytes across different inflammatory conditions in larvae. We resolved plasmatocytes into different states based on the expression of genes involved in cell cycle, antimicrobial response, and metabolism together with the identification of intermediate states. Further, we discovered rare subsets within crystal cells and lamellocytes that express fibroblast growth factor (FGF) ligand branchless and receptor breathless, respectively. We demonstrate that these FGF components are required for mediating effective immune responses against parasitoid wasp eggs, highlighting a novel role for FGF signaling in inter-hemocyte crosstalk. Our scRNA-seq analysis reveals the diversity of hemocytes and provides a rich resource of gene expression profiles for a systems-level understanding of their functions.

Data availability

Sequencing data have been deposited in GEO under the accession number GSE146596Elsewhere, data can be visualized at: www.flyrnai.org/scRNA/blood/Data code can accessed at: https://github.com/hbc/A-single-cell-survey-of-Drosophila-blood

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Sudhir Gopal Tattikota

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    For correspondence
    sudhir_gt@hms.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0318-5533
  2. Bumsik Cho

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    No competing interests declared.
  3. Yifang Liu

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  4. Yanhui Hu

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  5. Victor Barrera

    Biostatistics, Harvard T H Chan Bioinformatics Core, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0590-4634
  6. Michael J Steinbaugh

    Biostatistics, Harvard T H Chan Bioinformatics Core, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2403-2221
  7. Sang-Ho Yoon

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2611-5554
  8. Aram Comjean

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  9. Fangge Li

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  10. Franz Dervis

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  11. Ruei-Jiun Hung

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    Competing interests
    No competing interests declared.
  12. Jin-Wu Nam

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    No competing interests declared.
  13. Shannan Ho Sui

    Biostatistics, Harvard T H Chan Bioinformatics Core, Boston, United States
    Competing interests
    No competing interests declared.
  14. Jiwon Shim

    Department of Life Science, Hanyang University, Seoul, Republic of Korea
    Competing interests
    Jiwon Shim, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2409-1130
  15. Norbert Perrimon

    Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, United States
    For correspondence
    perrimon@receptor.med.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7542-472X

Funding

Samsung Science and Technology Foundation (SSTF-BA1701-15)

  • Jiwon Shim

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

Reviewing Editor

  1. Bruno Lemaître, École Polytechnique Fédérale de Lausanne, Switzerland

Publication history

  1. Received: December 30, 2019
  2. Accepted: May 8, 2020
  3. Accepted Manuscript published: May 12, 2020 (version 1)
  4. Version of Record published: May 19, 2020 (version 2)

Copyright

© 2020, Tattikota 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

  • 5,947
    Page views
  • 817
    Downloads
  • 45
    Citations

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

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. Sudhir Gopal Tattikota
  2. Bumsik Cho
  3. Yifang Liu
  4. Yanhui Hu
  5. Victor Barrera
  6. Michael J Steinbaugh
  7. Sang-Ho Yoon
  8. Aram Comjean
  9. Fangge Li
  10. Franz Dervis
  11. Ruei-Jiun Hung
  12. Jin-Wu Nam
  13. Shannan Ho Sui
  14. Jiwon Shim
  15. Norbert Perrimon
(2020)
A single-cell survey of Drosophila blood
eLife 9:e54818.
https://doi.org/10.7554/eLife.54818
  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
    Mariah L Hoye et al.
    Research Article

    Mutations in the RNA helicase, DDX3X, are a leading cause of Intellectual Disability and present as DDX3X syndrome, a neurodevelopmental disorder associated with cortical malformations and autism. Yet, the cellular and molecular mechanisms by which DDX3X controls cortical development are largely unknown. Here, using a mouse model of Ddx3x loss-of-function we demonstrate that DDX3X directs translational and cell cycle control of neural progenitors, which underlies precise corticogenesis. First, we show brain development is sensitive to Ddx3x dosage; complete Ddx3x loss from neural progenitors causes microcephaly in females, whereas hemizygous males and heterozygous females show reduced neurogenesis without marked microcephaly. In addition, Ddx3x loss is sexually dimorphic, as its paralog, Ddx3y, compensates for Ddx3x in the developing male neocortex. Using live imaging of progenitors, we show that DDX3X promotes neuronal generation by regulating both cell cycle duration and neurogenic divisions. Finally, we use ribosome profiling in vivo to discover the repertoire of translated transcripts in neural progenitors, including those which are DDX3X-dependent and essential for neurogenesis. Our study reveals invaluable new insights into the etiology of DDX3X syndrome, implicating dysregulated progenitor cell cycle dynamics and translation as pathogenic mechanisms.

    1. Developmental Biology
    2. Evolutionary Biology
    Mathi Thiruppathy et al.
    Short Report

    Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws.