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Molecular characterization of the sea lamprey retina illuminates the evolutionary origin of retinal cell types

Author

Listed:
  • Junqiang Wang

    (UCLA David Geffen School of Medicine)

  • Lin Zhang

    (UCLA David Geffen School of Medicine)

  • Martina Cavallini

    (UCLA David Geffen School of Medicine)

  • Ali Pahlevan

    (UCLA David Geffen School of Medicine)

  • Junwei Sun

    (UCLA David Geffen School of Medicine)

  • Ala Morshedian

    (UCLA David Geffen School of Medicine)

  • Gordon L. Fain

    (UCLA David Geffen School of Medicine)

  • Alapakkam P. Sampath

    (UCLA David Geffen School of Medicine)

  • Yi-Rong Peng

    (UCLA David Geffen School of Medicine)

Abstract

The lamprey, a primitive jawless vertebrate whose ancestors diverged from all other vertebrates over 500 million years ago, offers a unique window into the ancient formation of the retina. Using single-cell RNA-sequencing, we characterize retinal cell types in the lamprey and compare them to those in mouse, chicken, and zebrafish. We find six cell classes and 74 distinct cell types, many shared with other vertebrate species. The conservation of cell types indicates their emergence early in vertebrate evolution, highlighting primordial designs of retinal circuits for the rod pathway, ON-OFF discrimination, and direction selectivity. The diversification of amacrine and some ganglion cell types appears, however, to be distinct in the lamprey. We further infer genetic regulators in specifying retinal cell classes and identify ancestral regulatory elements across species, noting decreased conservation in specifying amacrine cells. Altogether, our characterization of the lamprey retina illuminates the evolutionary origin of visual processing in the retina.

Suggested Citation

  • Junqiang Wang & Lin Zhang & Martina Cavallini & Ali Pahlevan & Junwei Sun & Ala Morshedian & Gordon L. Fain & Alapakkam P. Sampath & Yi-Rong Peng, 2024. "Molecular characterization of the sea lamprey retina illuminates the evolutionary origin of retinal cell types," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55019-x
    DOI: 10.1038/s41467-024-55019-x
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    References listed on IDEAS

    as
    1. Bruce A. Rheaume & Amyeo Jereen & Mohan Bolisetty & Muhammad S. Sajid & Yue Yang & Kathleen Renna & Lili Sun & Paul Robson & Ephraim F. Trakhtenberg, 2018. "Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    2. Bruce A. Rheaume & Amyeo Jereen & Mohan Bolisetty & Muhammad S. Sajid & Yue Yang & Kathleen Renna & Lili Sun & Paul Robson & Ephraim F. Trakhtenberg, 2018. "Author Correction: Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    3. Joshua Hahn & Aboozar Monavarfeshani & Mu Qiao & Allison H. Kao & Yvonne Kölsch & Ayush Kumar & Vincent P. Kunze & Ashley M. Rasys & Rose Richardson & Joseph B. Wekselblatt & Herwig Baier & Robert J. , 2023. "Evolution of neuronal cell classes and types in the vertebrate retina," Nature, Nature, vol. 624(7991), pages 415-424, December.
    4. Jeremy N. Kay & Monica W. Chu & Joshua R. Sanes, 2012. "MEGF10 and MEGF11 mediate homotypic interactions required for mosaic spacing of retinal neurons," Nature, Nature, vol. 483(7390), pages 465-469, March.
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