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Cited by 146Neurobiology and Insect Physiology ResearchNeurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene Regulation

A Complete Developmental Sequence of a Drosophila Neuronal Lineage as Revealed by Twin-Spot MARCM

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Yu, Hung-Hsiang, Kao, Chih-Fei, He, Yisheng, Ding, Peng, Kao, Jui-Chun, Lee, Tzumin·2010·PLoS Biology
DOI 10.1371/journal.pbio.1000461PMC PMC2927434
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Abstract

Drosophila brains contain numerous neurons that form complex circuits. These neurons are derived in stereotyped patterns from a fixed number of progenitors, called neuroblasts, and identifying individual neurons made by a neuroblast facilitates the reconstruction of neural circuits. An improved MARCM (mosaic analysis with a repressible cell marker) technique, called twin-spot MARCM, allows one to label the sister clones derived from a common progenitor simultaneously in different colors. It enables identification of every single neuron in an extended neuronal lineage based on the order of neuron birth. Here we report the first example, to our knowledge, of complete lineage analysis among neurons derived from a common neuroblast that relay olfactory information from the antennal lobe (AL) to higher brain centers. By identifying the sequentially derived neurons, we found that the neuroblast serially makes 40 types of AL projection neurons (PNs). During embryogenesis, one PN with multi-glomerular innervation and 18 uniglomerular PNs targeting 17 glomeruli of the adult AL are born. Many more PNs of 22 additional types, including four types of polyglomerular PNs, derive after the neuroblast resumes dividing in early larvae. Although different offspring are generated in a rather arbitrary sequence, the birth order strictly dictates the fate of each post-mitotic neuron, including the fate of programmed cell death. Notably, the embryonic progenitor has an altered temporal identity following each self-renewing asymmetric cell division. After larval hatching, the same progenitor produces multiple neurons for each cell type, but the number of neurons for each type is tightly regulated. These observations substantiate the origin-dependent specification of neuron types. Sequencing neuronal lineages will not only unravel how a complex brain develops but also permit systematic identification of neuron types for detailed structure and function analysis of the brain.

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  • Primary neurons have significantly larger cell bodies and cell body fibres (from experimental evidence).

    “In cases in which experimental evidence exists27, primary neurons have significantly larger cell bodies and cell body fibres.”

    From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [27]

    The Discussion says that embryonic-born primary neurons elaborate extensively, but it does not compare their cell-body or fibre size with secondary neurons. The Results passage on cell bodies counts neurons rather than measuring their size. Searches for larger cell bodies and fibre diameter found no passage establishing the claimed significant difference. (LLM, conf=0.73)

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References 46 · Cited by 146

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Authors
Yu, H.-H., Kao, C.-F., He, Y., Ding, P., Kao, J.-C., & Lee, T.
Affiliations
  • Howard Hughes Medical Institute (US)
  • University of Massachusetts Chan Medical School (US)
Corresponding author
Lee, Tzumin
ORCID
Venue
PLoS Biology
Publisher
Public Library of Science (PLoS)
Published
2010-08-24
Volume
8
Issue
8
Pages
e1000461
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.1000461
PMC
PMC2927434
OpenAlex
W2135823825
Cited by
146
References
46
Citations by year
2026: 4 · 2025: 14 · 2024: 3 · 2023: 8 · 2022: 4 · 2021: 10 · 2020: 16 · 2019: 10 · 2018: 9 · 2017: 11 · 2016: 6 · 2015: 5 · 2014: 8 · 2013: 19 · 2012: 10
FWCI
4.92
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (MH080739)
  • National Institute of Mental Health (MH080739, R01MH080739)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
neuronal lineage, neuroblasts, Drosophila, olfactory glomeruli, asymmetric cell division, programmed cell death, neuronal fate specification, neural circuit reconstruction, temporal identity
MeSH terms
Animals, Brain, Clone Cells, Drosophila, Genetic Techniques, Mosaicism, Neurons, Olfactory Pathways, Cell Lineage, Neurogenesis

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