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

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 ne...

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Main Authors: 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
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/63450
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spelling doaj-52b08758320341fd9a60d8b91ca94a082021-05-05T22:40:21ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.63450Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neuronsQijing Xie0https://orcid.org/0000-0002-0997-8326Maria Brbic1Felix Horns2https://orcid.org/0000-0001-5872-5061Sai Saroja Kolluru3Robert C Jones4https://orcid.org/0000-0001-7235-9854Jiefu Li5https://orcid.org/0000-0002-0062-4652Anay R Reddy6Anthony Xie7Sayeh Kohani8Zhuoran Li9Colleen N McLaughlin10Tongchao Li11Chuanyun Xu12David Vacek13David J Luginbuhl14Jure Leskovec15Stephen R Quake16https://orcid.org/0000-0002-1613-0809Liqun Luo17https://orcid.org/0000-0001-5467-9264Hongjie Li18Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States; Neurosciences Graduate Program, Stanford University, Stanford, United StatesDepartment of Computer Science, Stanford University, Stanford, United StatesDepartment of Bioengineering, Stanford University, Stanford, United States; Biophysics Graduate Program, Stanford University, Stanford, United StatesDepartment of Bioengineering, Stanford University, Stanford, United StatesDepartment of Bioengineering, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Computer Science, Stanford University, Stanford, United StatesDepartment of Bioengineering, Stanford University, Stanford, United States; Department of Applied Physics, Stanford University, Stanford, United States; Chan Zuckerberg Biohub, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United StatesNeurons 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.https://elifesciences.org/articles/63450single-cellRNA sequencingneural developmentolfactory circuittranscriptomewiring
collection DOAJ
language English
format Article
sources DOAJ
author 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
spellingShingle 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
Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
eLife
single-cell
RNA sequencing
neural development
olfactory circuit
transcriptome
wiring
author_facet 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_sort Qijing Xie
title Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
title_short Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
title_full Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
title_fullStr Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
title_full_unstemmed Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
title_sort temporal evolution of single-cell transcriptomes of drosophila olfactory projection neurons
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-01-01
description 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.
topic single-cell
RNA sequencing
neural development
olfactory circuit
transcriptome
wiring
url https://elifesciences.org/articles/63450
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