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Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level

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Farmer, Andrew, Thibivilliers, Sandra, Ryu, Kook Hui, Schiefelbein, John, Libault, Marc·2021·Molecular Plant

Abstract

Similar to other complex organisms, plants consist of diverse and specialized cell types. The gain of unique biological functions of these different cell types is the consequence of the establishment of cell-type-specific transcriptional programs. As a necessary step in gaining a deeper understanding of the regulatory mechanisms controlling plant gene expression, we report the use of single-nucleus RNA sequencing (sNucRNA-seq) and single-nucleus assay for transposase accessible chromatin sequencing (sNucATAC-seq) technologies on Arabidopsis roots. The comparison of our single-nucleus transcriptomes to the published protoplast transcriptomes validated the use of nuclei as biological entities to establish plant cell-type-specific transcriptomes. Furthermore, our sNucRNA-seq results uncovered the transcriptomes of additional cell subtypes not identified by single-cell RNA-seq. Similar to our transcriptomic approach, the sNucATAC-seq approach led to the distribution of the Arabidopsis nuclei into distinct clusters, suggesting the differential accessibility of chromatin between groups of cells according to their identity. To reveal the impact of chromatin accessibility on gene expression, we integrated sNucRNA-seq and sNucATAC-seq data and demonstrated that cell-type-specific marker genes display cell-type-specific patterns of chromatin accessibility. Our data suggest that the differential chromatin accessibility is a critical mechanism to regulate gene activity at the cell-type level.

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Show all 8 references

Research works printed but not linked: 49

  1. Andersen, 2015, Suberization - the second life of an endodermal cell, Curr. Opin. Plant Biol., 28, 9, 10.1016/j.pbi.2015.08.004 · doi:10.1016/j.pbi.2015.08.004
  2. Arendt, 2019, Evolution of neuronal types and families, Curr. Opin. Neurobiol., 56, 144, 10.1016/j.conb.2019.01.022 · DOI
  3. Becht, 2019, Dimensionality reduction for visualizing single-cell data using UMAP, Nat. Biotechnol., 37, 38, 10.1038/nbt.4314 · DOI · Paper page
  4. Beisson, 2007, The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis, Plant Cell, 19, 351, 10.1105/tpc.106.048033 · DOI · Paper page
  5. Berhin, 2019, The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation, Cell, 176, 1367, 10.1016/j.cell.2019.01.005 · doi:10.1016/j.cell.2019.01.005
  6. Birnbaum, 2003, A gene expression map of the Arabidopsis root, Science, 302, 1956, 10.1126/science.1090022 · DOI · Paper page
  7. Bohme, 2004, The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth, Plant J., 40, 686, 10.1111/j.1365-313X.2004.02245.x · DOI
  8. Chen, 2015, The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and ENHANCER OF TRY AND CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots, J. Exp. Bot., 66, 4821, 10.1093/jxb/erv259 · DOI
  9. Deal, 2010, A simple method for gene expression and chromatin profiling of individual cell types within a tissue, Dev. Cell, 18, 1030, 10.1016/j.devcel.2010.05.013 · DOI · Paper page
  10. Del Toro-De Leon, 2019, Endosperm-specific transcriptome analysis by applying the INTACT system, Plant Reprod., 32, 55, 10.1007/s00497-018-00356-3 · DOI
  11. Denyer, 2019, Spatiotemporal developmental trajectories in the Arabidopsis root revealed using high-throughput single-cell RNA sequencing, Dev. Cell, 48, 840, 10.1016/j.devcel.2019.02.022 · DOI · Paper page
  12. Ding, 2019, Advances in plant GDSL lipases: from sequences to functional mechanisms, Acta Physiol. Plant, 41, 151, 10.1007/s11738-019-2944-4 · DOI
  13. Dominguez, 2015, Plant cutin genesis: unanswered questions, Trends Plant Sci., 20, 551, 10.1016/j.tplants.2015.05.009 · DOI
  14. Fendrych, 2014, Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis, Curr. Biol., 24, 931, 10.1016/j.cub.2014.03.025 · DOI · Paper page
  15. Gao, 2018, KIRA1 and ORESARA1 terminate flower receptivity by promoting cell death in the stigma of Arabidopsis, Nat. Plants, 4, 365, 10.1038/s41477-018-0160-7 · doi:10.1038/s41477-018-0160-7
  16. Girard, 2012, Tomato GDSL1 is required for cutin deposition in the fruit cuticle, Plant Cell, 24, 3119, 10.1105/tpc.112.101055 · doi:10.1105/tpc.112.101055
  17. Gulko, 2019, An evolutionary framework for measuring epigenomic information and estimating cell-type-specific fitness consequences, Nat. Genet., 51, 335, 10.1038/s41588-018-0300-z · DOI
  18. Heo, 2017, Differentiation of conductive cells: a matter of life and death, Curr. Opin. Plant Biol., 35, 23, 10.1016/j.pbi.2016.10.007 · DOI
  19. Hu, 2018, Single-nucleus transcriptomic survey of cell diversity and functional maturation in postnatal mammalian hearts, Genes Dev., 32, 1344, 10.1101/gad.316802.118 · DOI
  20. Jean-Baptiste, 2019, Dynamics of gene expression in single root cells of Arabidopsis thaliana, Plant Cell, 31, 993, 10.1105/tpc.18.00785 · DOI · Paper page
  21. Kumpf, 2015, The root cap: a short story of life and death, J. Exp. Bot., 66, 5651, 10.1093/jxb/erv295 · DOI
  22. Kwak, 2005, Positional signaling mediated by a receptor-like kinase in Arabidopsis, Science, 307, 1111, 10.1126/science.1105373 · doi:10.1126/science.1105373
  23. Lai, 2018, Principles of nucleosome organization revealed by single-cell micrococcal nuclease sequencing, Nature, 562, 281, 10.1038/s41586-018-0567-3 · DOI
  24. Lai, 2017, Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis, Plant Mol. Biol., 95, 181, 10.1007/s11103-017-0648-y · doi:10.1007/s11103-017-0648-y
  25. Li, 2007, Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers, Proc. Natl. Acad. Sci. U S A, 104, 18339, 10.1073/pnas.0706984104 · DOI · Paper page
  26. Li, 2007, Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin-associated acyltransferase, Plant Physiol., 144, 1267, 10.1104/pp.107.099432 · doi:10.1104/pp.107.099432
  27. Lu, 2017, Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes, Nucleic Acids Res., 45, e41, 10.1093/nar/gkw1179 · DOI · Paper page
  28. Maher, 2018, Profiling of accessible chromatin regions across multiple plant species and cell types reveals common gene regulatory principles and new control modules, Plant Cell, 30, 15, 10.1105/tpc.17.00581 · DOI · Paper page
  29. Norrie, 2019, Nucleome dynamics during retinal development, Neuron, 104, 512, 10.1016/j.neuron.2019.08.002 · DOI
  30. Olvera-Carrillo, 2015, A conserved Core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants, Plant Physiol., 169, 2684
  31. Palovaara, 2019, Adapting INTACT to analyse cell-type-specific transcriptomes and nucleocytoplasmic mRNA dynamics in the Arabidopsis embryo, Plant Reprod., 32, 113, 10.1007/s00497-018-0347-0 · DOI
  32. Park, 2010, Mutation in Wilted Dwarf and Lethal 1 (WDL1) causes abnormal cuticle formation and rapid water loss in rice, Plant Mol. Biol., 74, 91, 10.1007/s11103-010-9656-x · doi:10.1007/s11103-010-9656-x
  33. Pirrello, 2018, Transcriptome profiling of sorted endoreduplicated nuclei from tomato fruits: how the global shift in expression ascribed to DNA ploidy influences RNA-Seq data normalization and interpretation, Plant J., 93, 387, 10.1111/tpj.13783 · DOI
  34. Pott, 2015, Single-cell ATAC-seq: strength in numbers, Genome Biol., 16, 172, 10.1186/s13059-015-0737-7 · DOI
  35. Reynoso, 2018, Nuclear transcriptomes at high resolution using retooled INTACT, Plant Physiol., 176, 270, 10.1104/pp.17.00688 · doi:10.1104/pp.17.00688
  36. Ryu, 2019, Single-cell RNA sequencing resolves molecular relationships among individual plant cells, Plant Physiol., 179, 1444, 10.1104/pp.18.01482 · DOI · Paper page
  37. Salazar-Henao, 2016, The regulation and plasticity of root hair patterning and morphogenesis, Development, 143, 1848, 10.1242/dev.132845 · DOI · Paper page
  38. Sarkar, 2009, Plant cell walls throughout evolution: towards a molecular understanding of their design principles, J. Exp. Bot., 60, 3615, 10.1093/jxb/erp245 · DOI · Paper page
  39. Shulse, 2019, High-throughput single-cell transcriptome profiling of plant cell types, Cell Rep., 27, 2241, 10.1016/j.celrep.2019.04.054 · DOI · Paper page
  40. Sijacic, 2018, Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type-specific transcription factor networks, Plant J., 94, 215, 10.1111/tpj.13882 · DOI
  41. Sinnamon, 2019, The accessible chromatin landscape of the murine hippocampus at single-cell resolution, Genome Res., 29, 857, 10.1101/gr.243725.118 · DOI
  42. Somssich, 2016, Cell wall heterogeneity in root development of Arabidopsis, Front. Plant Sci., 7, 1242, 10.3389/fpls.2016.01242 · DOI
  43. Stuart, 2019, Comprehensive integration of single-cell data, Cell, 177, 1888, 10.1016/j.cell.2019.05.031 · DOI · Paper page
  44. Tannenbaum, 2018, Regulatory chromatin landscape in Arabidopsis thaliana roots uncovered by coupling INTACT and ATAC-seq, Plant Methods, 14, 113, 10.1186/s13007-018-0381-9 · DOI
  45. Tsukagoshi, 2010, Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root, Cell, 143, 606, 10.1016/j.cell.2010.10.020 · DOI · Paper page
  46. Turco, 2019, Molecular mechanisms driving switch behavior in xylem cell differentiation, Cell Rep., 28, 342, 10.1016/j.celrep.2019.06.041 · DOI
  47. Yu, 2015, ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization, Bioinformatics, 31, 2382, 10.1093/bioinformatics/btv145 · DOI · Paper page
  48. Zhang, 2019, A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root, Mol. Plant, 12, 648, 10.1016/j.molp.2019.04.004 · DOI · Paper page
  49. Zhou, 2019, Global prediction of chromatin accessibility using small-cell-number and single-cell RNA-seq, Nucleic Acids Res., 47, e121, 10.1093/nar/gkz716 · DOI

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Metadata

Authors
Farmer, A., Thibivilliers, S., Ryu, K. H., Schiefelbein, J., & Libault, M.
Venue
Molecular Plant
Publisher
Elsevier BV
Published
2021-03
Volume
14
Issue
3
Pages
372-383
ISSN
1674-2052 (ISSN-L)
OpenAlex
W3119669192
Cited by
317
References
8
FWCI
15.03
Type
journal article
Language
en
Open access
hybrid
Licence
Funders
  • National Science Foundation (IOS #1339194, IOS #1923589, 1854326)
  • U.S. Department of Energy (DE-SC0020358)

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CoChat. (2026). Citation check: Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level. https://app.cochat.ai/papers/10.1016/j.molp.2021.01.001
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Farmer, A., Thibivilliers, S., Ryu, K. H., Schiefelbein, J., & Libault, M. (2021). Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level. Molecular Plant. https://doi.org/10.1016/j.molp.2021.01.001

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