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Title: A single-cell Arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants

Journal Article · · Developmental Cell
 [1];  [2];  [3];  [4];  [3];  [5];  [5];  [5];  [6];  [5];  [7];  [8]
  1. Duke University, Durham, NC (United States); OSTI
  2. Humboldt University of Berlin (Germany); Max Delbrück Center for Molecular Medicine, Berlin (Germany)
  3. Duke University, Durham, NC (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. University of British Columbia, Vancouver, BC (Canada)
  6. Max Delbrück Center for Molecular Medicine, Berlin (Germany); Humboldt University of Berlin (Germany)
  7. Duke University, Durham, NC (United States); Duke Univ., Durham, NC (United States). Howard Hughes Medical Institute
  8. Humboldt University of Berlin (Germany); Max Delbrück Center for Molecular Medicine, Berlin (Germany); Humboldt University of Berlin (Germany)

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.

Research Organization:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
Burroughs Wellcome Fund; Canadian Institutes of Health Research (CIHR); German Research Foundation (DFG); Helmholtz Association; Howard Hughes Medical Institute; National Institutes of Health (NIH); National Science Foundation (NSF); Natural Sciences and Engineering Research Council of Canada (NSERC); New Frontiers in Research Fund (NFRF); US Department of Agriculture (USDA); USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1904100
Journal Information:
Developmental Cell, Journal Name: Developmental Cell Journal Issue: 4 Vol. 57; ISSN 1534-5807
Publisher:
Cell Press - ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (99)

Arabidopsis - Root cell types image January 2019
Optimizing RNA-Seq Mapping with STAR book January 2016
Characterization of SHORT-ROOT function in the Arabidopsis root vascular system journal July 2010
The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root journal August 1996
WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning journal November 1999
Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries journal April 1998
Emergence of a High-Plasticity Cell State during Lung Cancer Evolution journal August 2020
The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche journal October 2004
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape journal May 2016
Optimal-Transport Analysis of Single-Cell Gene Expression Identifies Developmental Trajectories in Reprogramming journal February 2019
Comprehensive Integration of Single-Cell Data journal June 2019
A Genome-Scale Resource for the Functional Characterization of Arabidopsis Transcription Factors journal July 2014
High-Throughput Single-Cell Transcriptome Profiling of Plant Cell Types journal May 2019
DoubletFinder: Doublet Detection in Single-Cell RNA Sequencing Data Using Artificial Nearest Neighbors journal April 2019
Pericycle journal May 2014
Rules and Self-Organizing Properties of Post-embryonic Plant Organ Cell Division Patterns journal February 2016
Strigolactone- and Karrikin-Independent SMXL Proteins Are Central Regulators of Phloem Formation journal April 2017
A bHLH Complex Controls Embryonic Vascular Tissue Establishment and Indeterminate Growth in Arabidopsis journal February 2013
High-Resolution Expression Map of the Arabidopsis Root Reveals Alternative Splicing and lincRNA Regulation journal November 2016
Spatiotemporal Developmental Trajectories in the Arabidopsis Root Revealed Using High-Throughput Single-Cell RNA Sequencing journal March 2019
A Single-Cell RNA Sequencing Profiles the Developmental Landscape of Arabidopsis Root journal May 2019
Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level journal March 2021
The promise of single-cell genomics in plants journal April 2020
Uncovering Gene Regulatory Networks Controlling Plant Cell Differentiation journal August 2017
Intricacies of single-cell multi-omics data integration journal February 2022
A map of cell type‐specific auxin responses journal January 2013
APL regulates vascular tissue identity in Arabidopsis journal November 2003
Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate journal April 2010
Near-optimal probabilistic RNA-seq quantification journal April 2016
Integrating single-cell transcriptomic data across different conditions, technologies, and species journal April 2018
Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks journal December 2019
The regulatory landscape of Arabidopsis thaliana roots at single-cell resolution journal June 2021
Minimum requirements for changing and maintaining endodermis cell identity in the Arabidopsis root journal July 2018
Integrative single-cell analysis journal January 2019
Mobile PEAR transcription factors integrate positional cues to prime cambial growth journal January 2019
The single-cell transcriptional landscape of mammalian organogenesis journal February 2019
Gene expression cartography journal November 2019
Generalizing RNA velocity to transient cell states through dynamical modeling journal August 2020
Orchestrating single-cell analysis with Bioconductor journal December 2019
Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana journal May 1998
Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots journal March 2006
Cell-specific nitrogen responses mediate developmental plasticity journal January 2008
The MYB36 transcription factor orchestrates Casparian strip formation journal June 2015
MYB36 regulates the transition from proliferation to differentiation in the Arabidopsis root journal September 2015
Framework for gradual progression of cell ontogeny in the Arabidopsis root meristem journal October 2017
Cortex proliferation in the root is a protective mechanism against abiotic stress journal May 2015
Reconstructing spatiotemporal gene expression data from partial observations journal July 2009
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Complex heatmaps reveal patterns and correlations in multidimensional genomic data journal May 2016
Feature specific quantile normalization enables cross-platform classification of molecular subtypes using gene expression data journal January 2018
The barcode, UMI, set format and BUStools journal May 2019
Measuring cell identity in noisy biological systems journal July 2011
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation journal January 2012
A Conceptual Framework for Cell Identity Transitions in Plants journal November 2017
A single-cell view of the transcriptome during lateral root initiation in Arabidopsis thaliana journal April 2021
Transcription switches for protoxylem and metaxylem vessel formation journal August 2005
Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division journal August 2004
Arabidopsis thickvein Mutation Affects Vein Thickness and Organ Vascularization, and Resides in a Provascular Cell-Specific Spermine Synthase Involved in Vein Definition and in Polar Auxin Transport journal May 2005
Combining Expression and Comparative Evolutionary Analysis. The COBRA Gene Family journal November 2006
SHORT-ROOT Regulates Primary, Lateral, and Adventitious Root Development in Arabidopsis journal October 2010
Genome-Wide Direct Target Analysis Reveals a Role for SHORT-ROOT in Root Vascular Patterning through Cytokinin Homeostasis     journal September 2011
Diversification of Root Hair Development Genes in Vascular Plants journal May 2017
A Comprehensive Toolkit for Inducible, Cell Type-Specific Gene Expression in Arabidopsis journal July 2018
Single-Cell RNA Sequencing Resolves Molecular Relationships Among Individual Plant Cells journal February 2019
Cell Pattern in the Arabidopsis Root Epidermis Determined by Lateral Inhibition with Feedback journal March 2002
Transcriptional Profile of the Arabidopsis Root Quiescent Center journal June 2005
SUMO E3 Ligase HIGH PLOIDY2 Regulates Endocycle Onset and Meristem Maintenance inArabidopsis    journal August 2009
The Arabidopsis LAZY1 Family Plays a Key Role in Gravity Signaling within Statocytes and in Branch Angle Control of Roots and Shoots journal August 2017
A Spatiotemporal DNA Endoploidy Map of the Arabidopsis Root Reveals Roles for the Endocycle in Root Development and Stress Adaptation journal August 2018
Dynamics of Gene Expression in Single Root Cells of Arabidopsis thaliana journal March 2019
SHORTROOT-Mediated Intercellular Signals Coordinate Phloem Development in Arabidopsis Roots journal February 2020
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing journal January 1995
Regression Shrinkage and Selection Via the Lasso journal January 1996
The iRoCS Toolbox - 3D analysis of the plant root apical meristem at cellular resolution journal February 2014
A Gene Expression Map of the Arabidopsis Root journal December 2003
An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants journal June 2007
A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns journal November 2007
Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress journal May 2008
Secreted Peptide Signals Required for Maintenance of Root Stem Cell Niche in Arabidopsis journal August 2010
Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis journal April 2018
The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution journal April 2018
Single-cell transcriptional diversity is a hallmark of developmental potential journal January 2020
Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions journal November 2020
Week-long imaging of cell divisions in the Arabidopsis root meristem journal March 2019
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Quantification of cell identity from single-cell gene expression profiles journal January 2015
The potential of single-cell profiling in plants journal April 2016
Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression journal December 2019
ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death journal June 2008
A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche journal July 2014
Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis journal September 1993
Cellular organisation of the Arabidopsis thaliana root journal September 1993
Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis journal November 2016
Developmental single-cell transcriptomics in the Lytechinus variegatus sea urchin embryo journal September 2021
gprofiler2 -- an R package for gene list functional enrichment analysis and namespace conversion toolset g:Profiler journal November 2020
Whole-Genome Analysis of the SHORT-ROOT Developmental Pathway in Arabidopsis journal May 2006
Optimal transport analysis reveals trajectories in steady-state systems journal December 2021
A quantitative analysis of stem cell homeostasis in the Arabidopsis columella root cap journal March 2015