A single-cell Arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants
In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expre...
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| Published in | Developmental cell Vol. 57; no. 4; pp. 543 - 560.e9 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
28.02.2022
Cell Press - Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single-cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single-cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development.
[Display omitted]
•scRNA-seq of >110,000 cells produced a comprehensive Arabidopsis root atlas•Gradual, overlapping waves of gene expression underlie development of all cell types•Developmental trajectories enable visualization of cell specification events•scRNA-seq of the scarecrow mutant reveals a cell identity change occurs over time
How do transcriptional networks regulate organ development? Using scRNA-seq, Shahan and Hsu et al. produced an Arabidopsis root atlas, revealing gradual gene expression changes underlying differentiation of cell types and candidate regulators of cell fate. The atlas enabled interpretation of smaller scRNA-seq datasets and revealed new phenotypes in developmental mutants. |
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| AbstractList | In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single-cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single-cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development. In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model to investigate the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single cell resolution, shortroot and scarecrow . We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow . Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development. How do transcriptional networks regulate organ development? Using scRNA-seq, Shahan and Hsu et al. produced an Arabidopsis root atlas, revealing gradual gene expression changes underlying differentiation of cell types and candidate regulators of cell fate. The atlas enabled interpretation of smaller scRNA-seq datasets and revealed new phenotypes in developmental mutants. In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single-cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single-cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development.In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single-cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single-cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development. In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model for investigating the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single-cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single-cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development. [Display omitted] •scRNA-seq of >110,000 cells produced a comprehensive Arabidopsis root atlas•Gradual, overlapping waves of gene expression underlie development of all cell types•Developmental trajectories enable visualization of cell specification events•scRNA-seq of the scarecrow mutant reveals a cell identity change occurs over time How do transcriptional networks regulate organ development? Using scRNA-seq, Shahan and Hsu et al. produced an Arabidopsis root atlas, revealing gradual gene expression changes underlying differentiation of cell types and candidate regulators of cell fate. The atlas enabled interpretation of smaller scRNA-seq datasets and revealed new phenotypes in developmental mutants. In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate growth, is an ideal model to investigate the spatiotemporal transcriptional signatures underlying developmental trajectories. To map gene expression dynamics across root cell types and developmental time, we built a comprehensive, organ-scale atlas at single cell resolution. In addition to estimating developmental progressions in pseudotime, we employed the mathematical concept of optimal transport to infer developmental trajectories and identify their underlying regulators. To demonstrate the utility of the atlas to interpret new datasets, we profiled mutants for two key transcriptional regulators at single cell resolution, shortroot and scarecrow. We report transcriptomic and in vivo evidence for tissue trans-differentiation underlying a mixed cell identity phenotype in scarecrow. Our results support the atlas as a rich community resource for unraveling the transcriptional programs that specify and maintain cell identity to regulate spatiotemporal organ development. |
| Author | Ohler, Uwe Cole, Benjamin J. Greenstreet, Laura Hsu, Che-Wei Nolan, Trevor M. Afanassiev, Anton Shahan, Rachel Taylor, Isaiah W. Zhang, Stephen Vlot, Anna Hendrika Cornelia Schiebinger, Geoffrey Benfey, Philip N. |
| AuthorAffiliation | 7 Howard Hughes Medical Institute, Duke University, Durham, North Carolina 27708, USA 5 Department of Mathematics, University of British Columbia, Vancouver, V6T 1Z2 British Columbia, Canada 6 Department of Computer Science, Humboldt Universität zu Berlin, 10117 Berlin, Germany 9 These authors contributed equally to this work 8 These authors contributed equally to this work 10 Corresponding authors 11 Lead contact 4 Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA 1 Department of Biology, Duke University, Durham, North Carolina 27708, USA 2 Department of Biology, Humboldt Universität zu Berlin, 10117 Berlin, Germany 3 The Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, 10115 Berlin, Germany |
| AuthorAffiliation_xml | – name: 7 Howard Hughes Medical Institute, Duke University, Durham, North Carolina 27708, USA – name: 8 These authors contributed equally to this work – name: 11 Lead contact – name: 1 Department of Biology, Duke University, Durham, North Carolina 27708, USA – name: 5 Department of Mathematics, University of British Columbia, Vancouver, V6T 1Z2 British Columbia, Canada – name: 6 Department of Computer Science, Humboldt Universität zu Berlin, 10117 Berlin, Germany – name: 3 The Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, 10115 Berlin, Germany – name: 9 These authors contributed equally to this work – name: 10 Corresponding authors – name: 2 Department of Biology, Humboldt Universität zu Berlin, 10117 Berlin, Germany – name: 4 Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA |
| Author_xml | – sequence: 1 givenname: Rachel surname: Shahan fullname: Shahan, Rachel organization: Department of Biology, Duke University, Durham, NC 27708, USA – sequence: 2 givenname: Che-Wei surname: Hsu fullname: Hsu, Che-Wei organization: Department of Biology, Humboldt Universität zu Berlin, 10117 Berlin, Germany – sequence: 3 givenname: Trevor M. surname: Nolan fullname: Nolan, Trevor M. organization: Department of Biology, Duke University, Durham, NC 27708, USA – sequence: 4 givenname: Benjamin J. surname: Cole fullname: Cole, Benjamin J. organization: Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA – sequence: 5 givenname: Isaiah W. surname: Taylor fullname: Taylor, Isaiah W. organization: Department of Biology, Duke University, Durham, NC 27708, USA – sequence: 6 givenname: Laura surname: Greenstreet fullname: Greenstreet, Laura organization: Department of Mathematics, University of British Columbia, Vancouver, BC V6T 1Z2, Canada – sequence: 7 givenname: Stephen surname: Zhang fullname: Zhang, Stephen organization: Department of Mathematics, University of British Columbia, Vancouver, BC V6T 1Z2, Canada – sequence: 8 givenname: Anton surname: Afanassiev fullname: Afanassiev, Anton organization: Department of Mathematics, University of British Columbia, Vancouver, BC V6T 1Z2, Canada – sequence: 9 givenname: Anna Hendrika Cornelia surname: Vlot fullname: Vlot, Anna Hendrika Cornelia organization: The Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, 10115 Berlin, Germany – sequence: 10 givenname: Geoffrey surname: Schiebinger fullname: Schiebinger, Geoffrey organization: Department of Mathematics, University of British Columbia, Vancouver, BC V6T 1Z2, Canada – sequence: 11 givenname: Philip N. surname: Benfey fullname: Benfey, Philip N. email: philip.benfey@duke.edu organization: Department of Biology, Duke University, Durham, NC 27708, USA – sequence: 12 givenname: Uwe surname: Ohler fullname: Ohler, Uwe email: uwe.ohler@mdc-berlin.de organization: Department of Biology, Humboldt Universität zu Berlin, 10117 Berlin, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35134336$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1904100$$D View this record in Osti.gov |
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| IngestDate | Thu Aug 21 18:24:50 EDT 2025 Thu Dec 05 06:22:29 EST 2024 Thu Jul 10 18:11:22 EDT 2025 Mon Jul 21 05:45:47 EDT 2025 Tue Jul 01 00:48:13 EDT 2025 Thu Apr 24 23:01:46 EDT 2025 Fri Feb 23 02:39:55 EST 2024 |
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| Issue | 4 |
| Keywords | scRNA-seq development Arabidopsis cell fate SCARECROW root transcriptomics SHORTROOT |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved. This work is licensed under a Creative Commons Attribution 4.0 International License, which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 USDOE Office of Science (SC) US Department of Agriculture (USDA) Natural Sciences and Engineering Research Council of Canada (NSERC) Canadian Institutes of Health Research (CIHR) Howard Hughes Medical Institute National Institutes of Health (NIH) Burroughs Wellcome Fund German Research Foundation (DFG) AC02-05CH11231; 1F32GM136030-01; 1R35GM131725; IOS-2010686; 2021-6703-35139 Helmholtz Association National Science Foundation (NSF) New Frontiers in Research Fund (NFRF) RS, C-WH, TMN, BJC, PNB, and UO conceptualized the experiments. RS, TMN, and IWT generated the scRNA-seq data. RS, C-WH, TMN, BJC, AHCV, LG, SZ, AA, and GS analyzed the data. RS performed confocal imaging. RS wrote the manuscript with input from all authors. GS, PNB, and UO supervised the experiments and analyses. Author Contributions |
| OpenAccessLink | https://www.sciencedirect.com/science/article/pii/S1534580722000338 |
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| PublicationTitle | Developmental cell |
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| Snippet | In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate... In all multicellular organisms, transcriptional networks orchestrate organ development. The Arabidopsis root, with its simple structure and indeterminate... |
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| SubjectTerms | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism BASIC BIOLOGICAL SCIENCES cell fate development Gene Expression Regulation, Plant - genetics Gene Expression Regulation, Plant - physiology Gene Regulatory Networks - genetics Gene Regulatory Networks - physiology Mutation - genetics Plant Roots - genetics Plant Roots - metabolism root SCARECROW scRNA-seq SHORTROOT Single-Cell Analysis - methods Transcription Factors - genetics Transcription Factors - metabolism Transcriptome - physiology transcriptomics |
| Title | A single-cell Arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants |
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