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

Qijing Xie, Maria Brbic, Felix Horns, Sai Saroja Kolluru, Robert C Jones, Jiefu Li, Anay R Reddy, Anthony Xie, Sayeh Kohani, Zhuoran Li, Colleen N McLaughlin, Tongchao Li, Chuanyun Xu, David Vacek, David J Luginbuhl, Jure Leskovec, Stephen R Quake, Liqun Luo, Hongjie Li
Author Information
  1. Qijing Xie: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States. ORCID
  2. Maria Brbic: Department of Computer Science, Stanford University, Stanford, United States.
  3. Felix Horns: Department of Bioengineering, Stanford University, Stanford, United States. ORCID
  4. Sai Saroja Kolluru: Department of Bioengineering, Stanford University, Stanford, United States.
  5. Robert C Jones: Department of Bioengineering, Stanford University, Stanford, United States. ORCID
  6. Jiefu Li: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States. ORCID
  7. Anay R Reddy: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  8. Anthony Xie: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  9. Sayeh Kohani: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  10. Zhuoran Li: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  11. Colleen N McLaughlin: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  12. Tongchao Li: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  13. Chuanyun Xu: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  14. David Vacek: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  15. David J Luginbuhl: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.
  16. Jure Leskovec: Department of Computer Science, Stanford University, Stanford, United States.
  17. Stephen R Quake: Department of Bioengineering, Stanford University, Stanford, United States. ORCID
  18. Liqun Luo: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States. ORCID
  19. Hongjie Li: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States.

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 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.

Keywords

Associated Data

GEO | GSE161228; GSE100058

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Grants

  1. K99 AG062746/NIA NIH HHS
  2. R01 DC005982/NIDCD NIH HHS
  3. /Howard Hughes Medical Institute
  4. 1K99AG062746/NIH HHS

MeSH Term

Animals
Drosophila melanogaster
Neurites
Olfactory Nerve
Single-Cell Analysis
Time Factors
Transcriptome