The regulatory landscape of Arabidopsis thaliana roots at single-cell resolution

Dorrity, Michael W.; Alexandre, Cristina; Hamm, Morgan O.; Vigil, Anna-Lena; Fields, Stanley; Queitsch, Christine; Cuperus, Josh T.

doi:10.1038/s41467-021-23675-y

Cited by 110 publications

(93 citation statements)

References 49 publications

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“…Importantly, single-cell ATAC-seq in plants proved highly effective for the detection of CRMs at single-cell resolution ( Marand et al, 2021 ), allowing the detection of cell-type-specific CRMs, even in lowly abundant cell types. Data from Arabidopsis and maize revealed that approximately one-third of detected ACRs are cell-type specific ( Dorrity et al, 2021 ; Marand et al, 2021 ). Notably, the latter were enriched for TFBSs of TFs expressed in these cells ( Dorrity et al, 2021 ; Marand et al, 2021 ).…”

Section: Identifying and Verifying Crms Individually And Genome-widementioning

confidence: 99%

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Cis-regulatory sequences in plants: Their importance, discovery, and future challenges

2021

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The identification and characterization of cis-regulatory DNA sequences and how they function to coordinate responses to developmental and environmental cues is of paramount importance to plant biology. Key to these regulatory processes are cis-regulatory modules (CRMs), which include enhancers and silencers. Despite the extraordinary advances in high-quality sequence assemblies and genome annotations, the identification and understanding of CRMs, and how they regulate gene expression, lag significantly behind. This is especially true for their distinguishing characteristics and activity states. Here, we review the current knowledge on CRMs and breakthrough technologies enabling identification, characterization, and validation of CRMs; we compare the genomic distributions of CRMs with respect to their target genes between different plant species, and discuss the role of transposable elements harboring CRMs in the evolution of gene expression. This is an exciting time to study cis-regulomes in plants; however, significant existing challenges need to be overcome to fully understand and appreciate the role of CRMs in plant biology and in crop improvement.

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Section: Identifying and Verifying Crms Individually And Genome-widementioning

confidence: 99%

“…Data from Arabidopsis and maize revealed that approximately one-third of detected ACRs are cell-type specific ( Dorrity et al, 2021 ; Marand et al, 2021 ). Notably, the latter were enriched for TFBSs of TFs expressed in these cells ( Dorrity et al, 2021 ; Marand et al, 2021 ).…”

Section: Identifying and Verifying Crms Individually And Genome-widementioning

confidence: 99%

Cis-regulatory sequences in plants: Their importance, discovery, and future challenges

2021

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“…Single-cell sequencing has ushered in a new era of biology where it is possible to characterize cell types and function with unprecedented detail. In plants, this has resulted in detailed single-cell RNA-seq and Assay for Transposase-Accessible Chromatin (scATAC-seq) datasets primarily on different organ types from well-studied model organisms ( Denyer et al, 2019 ; Ryu et al, 2019 ; Dorrity et al, 2021 ; Gujas et al, 2020 ; Marand et al, 2020 ; Song et al, 2020 ; Liu et al, 2020a , 2020b ; Chen et al, 2021 ; Lopez-Anido et al, 2021 ; Xu et al, 2021 ). Most plant studies to date start with protoplast isolation, which has the potential to miss some recalcitrant cell types and often require correction to control for transcriptional changes elicited by lengthy enzyme treatment and centrifugation steps ( Ryu et al, 2019 ; Cuperus, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

The genome and preliminary single-nuclei transcriptome ofLemna minutareveals mechanisms of invasiveness

et al. 2021

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The ability to trace every cell in some model organisms has led to the fundamental understanding of development and cellular function. However, in plants the complexity of cell number, organ size and developmental time makes this a challenge even in the diminutive model plant Arabidopsis (Arabidopsis thaliana). Duckweed, basal non-grass aquatic monocots, provide an opportunity to follow every cell of an entire plant due to their small size, reduced body plan, and fast clonal growth habit. Here we present a chromosome-resolved genome for the highly invasive Lesser Duckweed (Lemna minuta) and generate a preliminary cell atlas leveraging low cell coverage single-nuclei sequencing. We resolved the 360 megabase genome into 21 chromosomes, revealing a core non-redundant gene set with only the ancient tau whole genome duplication shared with all monocots, and paralog expansion as a result of tandem duplications related to phytoremediation. Leveraging SMARTseq2 single-nuclei sequencing, which provided higher gene coverage yet lower cell count, we profiled 269 nuclei covering 36.9% (8,457) of the L. minuta transcriptome. Since molecular validation was not possible in this non-model plant, we leveraged gene orthology with model organism single cell expression datasets, gene ontology, and cell trajectory analysis to define putative cell types. We found that the tissue that we computationally defined as mesophyll expressed high levels of elemental transport genes consistent with this tissue playing a role in L. minuta wastewater detoxification. The L. minuta genome and preliminary cell map provide a paradigm to decipher developmental genes and pathways for an entire plant.

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“…Recent development of droplet microfluidic device-based single-cell systems have enabled researchers to co-encapsulate individual cells or nuclei with barcode beads in nanoliter water-inoil emulsions, making it possible to perform sequencing at the single-cell level (Lareau et al, 2019;Satpathy et al, 2019). For example, single-cell ATAC-seq (scATAC-seq) assays based on the 10X Genomics Chromium system have been successfully applied to study cell-specific chromatin accessibility in plants (Dorrity et al, 2021;Farmer et al, 2021;Marand et al, 2021;Marand and Schmitz, 2022). However, these commercial single-cell assays often require specialized equipment, trained personnel, and are very expensive, making it difficult for an individual laboratory to perform in house.…”

Section: Introductionmentioning

confidence: 99%

A combinatorial indexing strategy for epigenomic profiling of plant single cells

Marand

Schmitz

et al. 2021

Preprint

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Understanding how cis-regulatory elements facilitate gene expression is a key question in biology. Recent advances in single-cell genomics have led to the discovery of cell-specific chromatin landscapes that underlie transcription programs. However, the high equipment and reagent costs of commercial systems limit their applications for many laboratories. In this study, we profiled the Arabidopsis root single-cell epigenome using a combinatorial index and dual PCR barcode strategy without the need of any specialized equipment. We generated chromatin accessibility profiles for 13,576 Arabidopsis thaliana root nuclei with an average of 12,784 unique Tn5 integrations per cell and 85% of the Tn5 insertions localizing to discrete accessible chromatin regions. Comparison with data generated from a commercial microfluidic platform revealed that our method is capable of unbiased identification of cell type-specific chromatin accessibility with improved throughput, quality, and efficiency. We anticipate that by removing cost, instrument, and other technical obstacles, this combinatorial indexing method will be a valuable tool for routine investigation of single-cell epigenomes and usher new insight into plant growth, development and their interactions with the environment.

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The regulatory landscape of Arabidopsis thaliana roots at single-cell resolution

Cited by 110 publications

References 49 publications

Cis-regulatory sequences in plants: Their importance, discovery, and future challenges

Cis-regulatory sequences in plants: Their importance, discovery, and future challenges

The genome and preliminary single-nuclei transcriptome ofLemna minutareveals mechanisms of invasiveness

A combinatorial indexing strategy for epigenomic profiling of plant single cells

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