Brassinosteroid gene regulatory networks at cellular resolution in the Arabidopsis root
Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to diff...
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| Published in | Science (American Association for the Advancement of Science) Vol. 379; no. 6639; p. eadf4721 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
31.03.2023
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| Subjects | |
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| Abstract | Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to different cell types and developmental stages of the
Arabidopsis
root, we identified the elongating cortex as a site where brassinosteroids trigger a shift from proliferation to elongation associated with increased expression of cell wall–related genes. Our analysis revealed
HOMEOBOX FROM ARABIDOPSIS THALIANA 7
(
HAT7
) and
GT-2-LIKE 1
(
GTL1
) as brassinosteroid-responsive transcription factors that regulate cortex cell elongation. These results establish the cortex as a site of brassinosteroid-mediated growth and unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation, which illuminates aspects of spatiotemporal hormone responses.
Hormones known as brassinosteroids affect many aspects of plant growth and development. Nolan
et al
. applied single-cell RNA sequencing to the roots of the small mustard plant Arabidopsis to study how brassinosteroids control the developmental shift that cells undergo as they cease proliferation and begin to elongate. The gene network involved drove altered expression of genes involved in cell wall biogenesis and organization. Two particular transcription factors were identified as regulators of cell elongation. —PJH
Single-cell RNA sequencing identifies the elongating root cortex as the site of brassinosteroid-dependent growth. |
|---|---|
| AbstractList | Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to different cell types and developmental stages of the
root, we identified the elongating cortex as a site where brassinosteroids trigger a shift from proliferation to elongation associated with increased expression of cell wall-related genes. Our analysis revealed
(
) and
(
) as brassinosteroid-responsive transcription factors that regulate cortex cell elongation. These results establish the cortex as a site of brassinosteroid-mediated growth and unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation, which illuminates aspects of spatiotemporal hormone responses. Hormonal control of root elongationHormones known as brassinosteroids affect many aspects of plant growth and development. Nolan et al. applied single-cell RNA sequencing to the roots of the small mustard plant Arabidopsis to study how brassinosteroids control the developmental shift that cells undergo as they cease proliferation and begin to elongate. The gene network involved drove altered expression of genes involved in cell wall biogenesis and organization. Two particular transcription factors were identified as regulators of cell elongation. —PJHINTRODUCTIONCells traverse a developmental landscape as they acquire identities and progress toward end-stage differentiation. Gene regulatory networks control this progression and must be tuned according to developmental stage, cell identity, and environmental conditions. Hormones play important roles in remodeling these networks, but it has been challenging to understand how cell identities, developmental states, and hormone responses influence one another. Brassinosteroids are plant steroid hormones that regulate diverse processes, including cell division and cell elongation. Brassinosteroids signal to activate BRI1-EMS-SUPPRESSOR 1 (BES1) and BRASSINAZOLE-RESISTANT 1 (BZR1) transcription factors, which direct gene regulatory networks to control thousands of genes. Modulating brassinosteroids can lead to different responses depending on the developmental context, but how the underlying gene regulatory networks vary in space and time is unclear.RATIONALESingle-cell RNA sequencing (scRNA-seq) is a powerful approach to investigate cell- and developmental stage–specific responses to stimuli, but most previous studies have focused on a single time point. In this work, we used time series scRNA-seq to delineate the gene regulatory networks controlling brassinosteroid response in the Arabidopsis root. We then confirmed the spatial and developmental models arising from single-cell analysis using tissue-specific gene manipulations.RESULTSWe defined brassinosteroid-responsive gene expression using time series scRNA-seq. This identified the elongating root cortex as a site of brassinosteroid-mediated gene expression. Reconstruction of cortex trajectories showed that brassinosteroids promote a shift from proliferation to elongation associated with increased expression of cell wall–related genes. Accordingly, loss of brassinosteroid signaling in the cortex using a tissue-specific CRISPR approach impaired cell expansion in the elongation zone but had little effect on meristem cell length.To discover regulators of spatiotemporal brassinosteroid responses, we inferred gene regulatory networks across each cell type, developmental stage, and time point of our brassinosteroid time series. Our gene regulatory networks and experimental analysis revealed HOMEOBOX FROM ARABIDOPSIS THALIANA 7 (HAT7) and GT-2-LIKE 1 (GTL1) as brassinosteroid-responsive transcription factors that regulate cell elongation in the cortex. BES1 and GTL1 interact and control a common set of targets induced by brassinosteroids, as evidenced by misregulation in scRNA-seq of gtl1 df1 mutants. These datasets represent 210,856 single-cell transcriptomes, providing a high-resolution view of brassinosteroid-mediated gene regulatory networks.CONCLUSIONWe have established the cortex as a site for brassinosteroid-mediated gene expression, where brassinosteroids activate cell wall–related genes and promote elongation. We further showed that HAT7 and GTL1 are brassinosteroid-induced regulators along cortex trajectories that control cell elongation. These findings highlight the ability of scRNA-seq to identify context-specific transcription factors, which could be leveraged to precisely engineer plant growth and development. Our results unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation in the cortex, illuminating a spatiotemporal brassinosteroid response. Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to different cell types and developmental stages of the Arabidopsis root, we identified the elongating cortex as a site where brassinosteroids trigger a shift from proliferation to elongation associated with increased expression of cell wall-related genes. Our analysis revealed HOMEOBOX FROM ARABIDOPSIS THALIANA 7 (HAT7) and GT-2-LIKE 1 (GTL1) as brassinosteroid-responsive transcription factors that regulate cortex cell elongation. These results establish the cortex as a site of brassinosteroid-mediated growth and unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation, which illuminates aspects of spatiotemporal hormone responses.Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to different cell types and developmental stages of the Arabidopsis root, we identified the elongating cortex as a site where brassinosteroids trigger a shift from proliferation to elongation associated with increased expression of cell wall-related genes. Our analysis revealed HOMEOBOX FROM ARABIDOPSIS THALIANA 7 (HAT7) and GT-2-LIKE 1 (GTL1) as brassinosteroid-responsive transcription factors that regulate cortex cell elongation. These results establish the cortex as a site of brassinosteroid-mediated growth and unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation, which illuminates aspects of spatiotemporal hormone responses. Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that vary in space and time. By using time series single-cell RNA sequencing to profile brassinosteroid-responsive gene expression specific to different cell types and developmental stages of the Arabidopsis root, we identified the elongating cortex as a site where brassinosteroids trigger a shift from proliferation to elongation associated with increased expression of cell wall–related genes. Our analysis revealed HOMEOBOX FROM ARABIDOPSIS THALIANA 7 ( HAT7 ) and GT-2-LIKE 1 ( GTL1 ) as brassinosteroid-responsive transcription factors that regulate cortex cell elongation. These results establish the cortex as a site of brassinosteroid-mediated growth and unveil a brassinosteroid signaling network regulating the transition from proliferation to elongation, which illuminates aspects of spatiotemporal hormone responses. Hormones known as brassinosteroids affect many aspects of plant growth and development. Nolan et al . applied single-cell RNA sequencing to the roots of the small mustard plant Arabidopsis to study how brassinosteroids control the developmental shift that cells undergo as they cease proliferation and begin to elongate. The gene network involved drove altered expression of genes involved in cell wall biogenesis and organization. Two particular transcription factors were identified as regulators of cell elongation. —PJH Single-cell RNA sequencing identifies the elongating root cortex as the site of brassinosteroid-dependent growth. |
| Author | Ohler, Uwe Russinova, Eugenia Zhang, Jingyuan Taylor, Isaiah W. Wang, Ping Benfey, Philip N. Brosnan, Aiden Heitz, Matthieu Yin, Yanhai Szekely, Pablo Greenstreet, Laura Nolan, Trevor M. Vukašinović, Nemanja Hsu, Che-Wei Afanassiev, Anton Shahan, Rachel Schiebinger, Geoffrey Vanhoutte, Isabelle |
| Author_xml | – sequence: 1 givenname: Trevor M. orcidid: 0000-0003-1362-2557 surname: Nolan fullname: Nolan, Trevor M. organization: Department of Biology, Duke University, Durham, NC, USA – sequence: 2 givenname: Nemanja orcidid: 0000-0003-2740-7874 surname: Vukašinović fullname: Vukašinović, Nemanja organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium., Center for Plant Systems Biology, VIB, Ghent, Belgium – sequence: 3 givenname: Che-Wei orcidid: 0000-0003-3709-9748 surname: Hsu fullname: Hsu, Che-Wei organization: Department of Biology, Duke University, Durham, NC, USA., Department of Biology, Humboldt Universitat zu Berlin, Berlin, Germany., The Berlin Institute for Medical Systems Biology, Max Delbruck Center for Molecular Medicine, Berlin, Germany – sequence: 4 givenname: Jingyuan surname: Zhang fullname: Zhang, Jingyuan organization: Department of Biology, Duke University, Durham, NC, USA – sequence: 5 givenname: Isabelle orcidid: 0000-0003-2878-134X surname: Vanhoutte fullname: Vanhoutte, Isabelle organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium., Center for Plant Systems Biology, VIB, Ghent, Belgium – sequence: 6 givenname: Rachel orcidid: 0000-0001-7702-9432 surname: Shahan fullname: Shahan, Rachel organization: Department of Biology, Duke University, Durham, NC, USA., Howard Hughes Medical Institute, Duke University, Durham, NC, USA – sequence: 7 givenname: Isaiah W. orcidid: 0000-0002-6535-8658 surname: Taylor fullname: Taylor, Isaiah W. organization: Department of Biology, Duke University, Durham, NC, USA – sequence: 8 givenname: Laura orcidid: 0000-0003-0635-3870 surname: Greenstreet fullname: Greenstreet, Laura organization: Department of Mathematics, University of British Columbia, Vancouver, BC, Canada – sequence: 9 givenname: Matthieu orcidid: 0000-0003-1552-1688 surname: Heitz fullname: Heitz, Matthieu organization: Department of Mathematics, University of British Columbia, Vancouver, BC, Canada – sequence: 10 givenname: Anton surname: Afanassiev fullname: Afanassiev, Anton organization: Department of Mathematics, University of British Columbia, Vancouver, BC, Canada – sequence: 11 givenname: Ping orcidid: 0000-0002-4484-6329 surname: Wang fullname: Wang, Ping organization: Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA, USA – sequence: 12 givenname: Pablo orcidid: 0000-0002-1569-4151 surname: Szekely fullname: Szekely, Pablo organization: Department of Biology, Duke University, Durham, NC, USA., Howard Hughes Medical Institute, Duke University, Durham, NC, USA – sequence: 13 givenname: Aiden orcidid: 0000-0002-9979-4060 surname: Brosnan fullname: Brosnan, Aiden organization: Department of Biology, Duke University, Durham, NC, USA – sequence: 14 givenname: Yanhai orcidid: 0000-0002-3044-9701 surname: Yin fullname: Yin, Yanhai organization: Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA, USA – sequence: 15 givenname: Geoffrey surname: Schiebinger fullname: Schiebinger, Geoffrey organization: Department of Mathematics, University of British Columbia, Vancouver, BC, Canada – sequence: 16 givenname: Uwe orcidid: 0000-0002-0881-3116 surname: Ohler fullname: Ohler, Uwe organization: Department of Biology, Humboldt Universitat zu Berlin, Berlin, Germany., Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA, USA., Department of Computer Science, Humboldt Universitat zu Berlin, Berlin, Germany – sequence: 17 givenname: Eugenia orcidid: 0000-0002-0569-1977 surname: Russinova fullname: Russinova, Eugenia organization: Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium., Center for Plant Systems Biology, VIB, Ghent, Belgium – sequence: 18 givenname: Philip N. orcidid: 0000-0001-5302-758X surname: Benfey fullname: Benfey, Philip N. organization: Department of Biology, Duke University, Durham, NC, USA., Howard Hughes Medical Institute, Duke University, Durham, NC, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36996230$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works |
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| Snippet | Brassinosteroids are plant steroid hormones that regulate diverse processes, such as cell division and cell elongation, through gene regulatory networks that... Hormonal control of root elongationHormones known as brassinosteroids affect many aspects of plant growth and development. Nolan et al. applied single-cell RNA... |
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| SubjectTerms | Arabidopsis Arabidopsis - cytology Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - metabolism Brassinosteroids Brassinosteroids - metabolism Cell culture Cell Differentiation - genetics Cell division Cell Division - genetics Cell proliferation Cell walls Cellular communication Context CRISPR Developmental stages Elongation Environmental conditions Feedback (Response) Gene expression Gene Expression Regulation, Plant Gene Regulatory Networks Gene sequencing Genes Homeobox Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Hormones Individualized Instruction Meristems Mustard Networks Plant growth Plant Growth Regulators - metabolism Plant Roots - cytology Plant Roots - genetics Plant Roots - growth & development Resistance factors Ribonucleic acid RNA Signaling Steroid hormones Time series Trajectory control Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptomes |
| Title | Brassinosteroid gene regulatory networks at cellular resolution in the Arabidopsis root |
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