1. Neuroscience

Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons

  1. Qijing Xie
  2. Maria Brbic
  3. Felix Horns
  4. Sai Saroja Kolluru
  5. Robert C Jones
  6. Jiefu Li
  7. Anay R Reddy
  8. Anthony Xie
  9. Sayeh Kohani
  10. Zhuoran Li
  11. Colleen N McLaughlin
  12. Tongchao Li
  13. Chuanyun Xu
  14. David Vacek
  15. David J Luginbuhl
  16. Jure Leskovec
  17. Stephen R Quake  Is a corresponding author
  18. Liqun Luo  Is a corresponding author
  19. Hongjie Li
  1. Howard Hughes Medical Institute, Stanford University, United States
  2. Stanford University, United States
  3. Chan Zuckerberg Biohub, United States
https://doi.org/10.7554/eLife.63450
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  1. Qijing Xie
  2. Maria Brbic
  3. Felix Horns
  4. Sai Saroja Kolluru
  5. Robert C Jones
  6. Jiefu Li
  7. Anay R Reddy
  8. Anthony Xie
  9. Sayeh Kohani
  10. Zhuoran Li
  11. Colleen N McLaughlin
  12. Tongchao Li
  13. Chuanyun Xu
  14. David Vacek
  15. David J Luginbuhl
  16. Jure Leskovec
  17. Stephen R Quake
  18. Liqun Luo
  19. Hongjie Li
(2021)
Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
eLife 10:e63450.
https://doi.org/10.7554/eLife.63450
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Abstract

Neurons undergo substantial morphological and functional changes during development to form precise synaptic connections and acquire specific physiological properties. What are the underlying transcriptomic bases? Here, we obtained the single-cell transcriptomes of Drosophila olfactory projection neurons (PNs) at four developmental stages. We decoded the identity of 21 transcriptomic clusters corresponding to 20 PN types and developed methods to match transcriptomic clusters representing the same PN type across development. We discovered that PN transcriptomes reflect unique biological processes unfolding at each stage—neurite growth and pruning during metamorphosis at an early pupal stage; peaked transcriptomic diversity during olfactory circuit assembly at mid-pupal stages; and neuronal signaling in adults. At early developmental stages, PN types with adjacent birth order share similar transcriptomes. Together, our work reveals principles of cellular diversity during brain development and provides a resource for future studies of neural development in PNs and other neuronal types.

Data availability

Raw sequencing reads and preprocessed sequence data have been deposited in GEO under accession code GSE161228.

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

Article and author information

Author details

  1. Qijing Xie

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Maria Brbic

    Department of Computer Science, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Felix Horns

    Biophysics Graduate Program, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5872-5061

  4. Sai Saroja Kolluru

    Department of Bioengineering, Chan Zuckerberg Biohub, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Robert C Jones

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7235-9854

  6. Jiefu Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0062-4652

  7. Anay R Reddy

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Anthony Xie

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Sayeh Kohani

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  10. Zhuoran Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. Colleen N McLaughlin

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  12. Tongchao Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  13. Chuanyun Xu

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  14. David Vacek

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  15. David J Luginbuhl

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  16. Jure Leskovec

    Department of Computer Science, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  17. Stephen R Quake

    Chan Zuckerberg Biohub, San Francisco, United States
    For correspondence
    steve@quake-lab.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1613-0809

  18. Liqun Luo

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    For correspondence
    lluo@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5467-9264

  19. Hongjie Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01 DC005982)

  • Liqun Luo

National Institutes of Health (1K99AG062746)

  • Hongjie Li

Howard Hughes Medical Institute

  • Liqun Luo

Stanford University (Graduate Student Fellowship)

  • Qijing Xie

Wu Tsai Neuroscience Institute at Stanford (Interdisciplinary postdoctoral scholar)

  • Hongjie Li

We Tsai Neuroscience Institute at Stanford (Neuro-omics program)

  • Liqun Luo

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

Copyright

© 2021, Xie 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.

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  1. Qijing Xie
  2. Maria Brbic
  3. Felix Horns
  4. Sai Saroja Kolluru
  5. Robert C Jones
  6. Jiefu Li
  7. Anay R Reddy
  8. Anthony Xie
  9. Sayeh Kohani
  10. Zhuoran Li
  11. Colleen N McLaughlin
  12. Tongchao Li
  13. Chuanyun Xu
  14. David Vacek
  15. David J Luginbuhl
  16. Jure Leskovec
  17. Stephen R Quake
  18. Liqun Luo
  19. Hongjie Li
(2021)
Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
eLife 10:e63450.
https://doi.org/10.7554/eLife.63450

Share this article

https://doi.org/10.7554/eLife.63450

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Further reading

    1. Neuroscience

    Single-cell transcriptomes of developing and adult olfactory receptor neurons in Drosophila

    Colleen N McLaughlin, Maria Brbić ... Hongjie Li
    Research Article

    Recognition of environmental cues is essential for the survival of all organisms. Transcriptional changes occur to enable the generation and function of the neural circuits underlying sensory perception. To gain insight into these changes, we generated single-cell transcriptomes of Drosophila olfactory- (ORNs), thermo-, and hygro-sensory neurons at an early developmental and adult stage using single-cell and single-nucleus RNA sequencing. We discovered that ORNs maintain expression of the same olfactory receptors across development. Using receptor expression and computational approaches, we matched transcriptomic clusters corresponding to anatomically and physiologically defined neuron types across multiple developmental stages. We found that cell-type-specific transcriptomes partly reflected axon trajectory choices in development and sensory modality in adults. We uncovered stage-specific genes that could regulate the wiring and sensory responses of distinct ORN types. Collectively, our data reveal transcriptomic features of sensory neuron biology and provide a resource for future studies of their development and physiology.