BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin: mediated responses in arabidopsis

Rafal Archacki; Daniel Buszewicz; Tomasz J Sarnowski; Elzbieta Sarnowska; Anna T Rolicka; Takayuki Tohge; Alisdair R Fernie; Yusuke Jikumaru; Maciej Kotlinski; Roksana Iwanicka-Nowicka; Katarzyna Kalisiak; Jacek Patryn; Joanna Halibart-Puzio; Yuji Kamiya; Seth J Davis; Marta K Koblowska; Andrzej Jerzmanowski

doi:10.1371/journal.pone.0058588

BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin: mediated responses in arabidopsis

Rafal Archacki, Daniel Buszewicz, Tomasz J Sarnowski, Elzbieta Sarnowska, Anna T Rolicka, Takayuki Tohge, Alisdair R Fernie, Yusuke Jikumaru, Maciej Kotlinski, Roksana Iwanicka-Nowicka, Katarzyna Kalisiak, Jacek Patryn, Joanna Halibart-Puzio, Yuji Kamiya, Seth J Davis, Marta K Koblowska, Andrzej Jerzmanowski

Biology

Research output: Contribution to journal › Article › peer-review

Abstract

SWI/SNF chromatin remodeling complexes perform a pivotal function in the regulation of eukaryotic gene expression. Arabidopsis (Arabidopsis thaliana) mutants in major SWI/SNF subunits display embryo-lethal or dwarf phenotypes, indicating their critical role in molecular pathways controlling development and growth. As gibberellins (GA) are major positive regulators of plant growth, we wanted to establish whether there is a link between SWI/SNF and GA signaling in Arabidopsis. This study revealed that in brm-1 plants, depleted in SWI/SNF BRAHMA (BRM) ATPase, a number of GA-related phenotypic traits are GA-sensitive and that the loss of BRM results in markedly decreased level of endogenous bioactive GA. Transcriptional profiling of brm-1 and the GA biosynthesis mutant ga1-3, as well as the ga1-3/brm-1 double mutant demonstrated that BRM affects the expression of a large set of GA-responsive genes including genes responsible for GA biosynthesis and signaling. Furthermore, we found that BRM acts as an activator and directly associates with promoters of GA3ox1, a GA biosynthetic gene, and SCL3, implicated in positive regulation of the GA pathway. Many GA-responsive gene expression alterations in the brm-1 mutant are likely due to depleted levels of active GAs. However, the analysis of genetic interactions between BRM and the DELLA GA pathway repressors, revealed that BRM also acts on GA-responsive genes independently of its effect on GA level. Given the central position occupied by SWI/SNF complexes within regulatory networks controlling fundamental biological processes, the identification of diverse functional intersections of BRM with GA-dependent processes in this study suggests a role for SWI/SNF in facilitating crosstalk between GA-mediated regulation and other cellular pathways.

Original language	English
Article number	e58588
Pages (from-to)	1-12
Number of pages	12
Journal	PLoS ONE
Volume	8
Issue number	3
DOIs	https://doi.org/10.1371/journal.pone.0058588
Publication status	Published - 11 Mar 2013

Bibliographical note

Keywords

Adenosine Triphosphatases
Arabidopsis
Arabidopsis Proteins
Catalytic Domain
Chromatin Assembly and Disassembly
Chromosomal Proteins, Non-Histone
Gene Expression Profiling
Gene Expression Regulation, Plant
Gibberellins
Molecular Sequence Annotation
Mutation
Phenotype
Plant Growth Regulators
Promoter Regions, Genetic
Quantitative Trait, Heritable
Signal Transduction
Transcription Factors
Triazoles

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Cite this

Archacki, R., Buszewicz, D., Sarnowski, T. J., Sarnowska, E., Rolicka, A. T., Tohge, T., Fernie, A. R., Jikumaru, Y., Kotlinski, M., Iwanicka-Nowicka, R., Kalisiak, K., Patryn, J., Halibart-Puzio, J., Kamiya, Y., Davis, S. J., Koblowska, M. K., & Jerzmanowski, A. (2013). BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin: mediated responses in arabidopsis. PLoS ONE, 8(3), 1-12. Article e58588. https://doi.org/10.1371/journal.pone.0058588

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title = "BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin: mediated responses in arabidopsis",

abstract = "SWI/SNF chromatin remodeling complexes perform a pivotal function in the regulation of eukaryotic gene expression. Arabidopsis (Arabidopsis thaliana) mutants in major SWI/SNF subunits display embryo-lethal or dwarf phenotypes, indicating their critical role in molecular pathways controlling development and growth. As gibberellins (GA) are major positive regulators of plant growth, we wanted to establish whether there is a link between SWI/SNF and GA signaling in Arabidopsis. This study revealed that in brm-1 plants, depleted in SWI/SNF BRAHMA (BRM) ATPase, a number of GA-related phenotypic traits are GA-sensitive and that the loss of BRM results in markedly decreased level of endogenous bioactive GA. Transcriptional profiling of brm-1 and the GA biosynthesis mutant ga1-3, as well as the ga1-3/brm-1 double mutant demonstrated that BRM affects the expression of a large set of GA-responsive genes including genes responsible for GA biosynthesis and signaling. Furthermore, we found that BRM acts as an activator and directly associates with promoters of GA3ox1, a GA biosynthetic gene, and SCL3, implicated in positive regulation of the GA pathway. Many GA-responsive gene expression alterations in the brm-1 mutant are likely due to depleted levels of active GAs. However, the analysis of genetic interactions between BRM and the DELLA GA pathway repressors, revealed that BRM also acts on GA-responsive genes independently of its effect on GA level. Given the central position occupied by SWI/SNF complexes within regulatory networks controlling fundamental biological processes, the identification of diverse functional intersections of BRM with GA-dependent processes in this study suggests a role for SWI/SNF in facilitating crosstalk between GA-mediated regulation and other cellular pathways.",

keywords = "Adenosine Triphosphatases, Arabidopsis, Arabidopsis Proteins, Catalytic Domain, Chromatin Assembly and Disassembly, Chromosomal Proteins, Non-Histone, Gene Expression Profiling, Gene Expression Regulation, Plant, Gibberellins, Molecular Sequence Annotation, Mutation, Phenotype, Plant Growth Regulators, Promoter Regions, Genetic, Quantitative Trait, Heritable, Signal Transduction, Transcription Factors, Triazoles",

author = "Rafal Archacki and Daniel Buszewicz and Sarnowski, {Tomasz J} and Elzbieta Sarnowska and Rolicka, {Anna T} and Takayuki Tohge and Fernie, {Alisdair R} and Yusuke Jikumaru and Maciej Kotlinski and Roksana Iwanicka-Nowicka and Katarzyna Kalisiak and Jacek Patryn and Joanna Halibart-Puzio and Yuji Kamiya and Davis, {Seth J} and Koblowska, {Marta K} and Andrzej Jerzmanowski",

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Archacki, R, Buszewicz, D, Sarnowski, TJ, Sarnowska, E, Rolicka, AT, Tohge, T, Fernie, AR, Jikumaru, Y, Kotlinski, M, Iwanicka-Nowicka, R, Kalisiak, K, Patryn, J, Halibart-Puzio, J, Kamiya, Y, Davis, SJ, Koblowska, MK & Jerzmanowski, A 2013, 'BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin: mediated responses in arabidopsis', PLoS ONE, vol. 8, no. 3, e58588, pp. 1-12. https://doi.org/10.1371/journal.pone.0058588

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T2 - mediated responses in arabidopsis

AU - Archacki, Rafal

AU - Buszewicz, Daniel

AU - Sarnowski, Tomasz J

AU - Sarnowska, Elzbieta

AU - Rolicka, Anna T

AU - Tohge, Takayuki

AU - Fernie, Alisdair R

AU - Jikumaru, Yusuke

AU - Kotlinski, Maciej

AU - Iwanicka-Nowicka, Roksana

AU - Kalisiak, Katarzyna

AU - Patryn, Jacek

AU - Halibart-Puzio, Joanna

AU - Kamiya, Yuji

AU - Davis, Seth J

AU - Koblowska, Marta K

AU - Jerzmanowski, Andrzej

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N2 - SWI/SNF chromatin remodeling complexes perform a pivotal function in the regulation of eukaryotic gene expression. Arabidopsis (Arabidopsis thaliana) mutants in major SWI/SNF subunits display embryo-lethal or dwarf phenotypes, indicating their critical role in molecular pathways controlling development and growth. As gibberellins (GA) are major positive regulators of plant growth, we wanted to establish whether there is a link between SWI/SNF and GA signaling in Arabidopsis. This study revealed that in brm-1 plants, depleted in SWI/SNF BRAHMA (BRM) ATPase, a number of GA-related phenotypic traits are GA-sensitive and that the loss of BRM results in markedly decreased level of endogenous bioactive GA. Transcriptional profiling of brm-1 and the GA biosynthesis mutant ga1-3, as well as the ga1-3/brm-1 double mutant demonstrated that BRM affects the expression of a large set of GA-responsive genes including genes responsible for GA biosynthesis and signaling. Furthermore, we found that BRM acts as an activator and directly associates with promoters of GA3ox1, a GA biosynthetic gene, and SCL3, implicated in positive regulation of the GA pathway. Many GA-responsive gene expression alterations in the brm-1 mutant are likely due to depleted levels of active GAs. However, the analysis of genetic interactions between BRM and the DELLA GA pathway repressors, revealed that BRM also acts on GA-responsive genes independently of its effect on GA level. Given the central position occupied by SWI/SNF complexes within regulatory networks controlling fundamental biological processes, the identification of diverse functional intersections of BRM with GA-dependent processes in this study suggests a role for SWI/SNF in facilitating crosstalk between GA-mediated regulation and other cellular pathways.

AB - SWI/SNF chromatin remodeling complexes perform a pivotal function in the regulation of eukaryotic gene expression. Arabidopsis (Arabidopsis thaliana) mutants in major SWI/SNF subunits display embryo-lethal or dwarf phenotypes, indicating their critical role in molecular pathways controlling development and growth. As gibberellins (GA) are major positive regulators of plant growth, we wanted to establish whether there is a link between SWI/SNF and GA signaling in Arabidopsis. This study revealed that in brm-1 plants, depleted in SWI/SNF BRAHMA (BRM) ATPase, a number of GA-related phenotypic traits are GA-sensitive and that the loss of BRM results in markedly decreased level of endogenous bioactive GA. Transcriptional profiling of brm-1 and the GA biosynthesis mutant ga1-3, as well as the ga1-3/brm-1 double mutant demonstrated that BRM affects the expression of a large set of GA-responsive genes including genes responsible for GA biosynthesis and signaling. Furthermore, we found that BRM acts as an activator and directly associates with promoters of GA3ox1, a GA biosynthetic gene, and SCL3, implicated in positive regulation of the GA pathway. Many GA-responsive gene expression alterations in the brm-1 mutant are likely due to depleted levels of active GAs. However, the analysis of genetic interactions between BRM and the DELLA GA pathway repressors, revealed that BRM also acts on GA-responsive genes independently of its effect on GA level. Given the central position occupied by SWI/SNF complexes within regulatory networks controlling fundamental biological processes, the identification of diverse functional intersections of BRM with GA-dependent processes in this study suggests a role for SWI/SNF in facilitating crosstalk between GA-mediated regulation and other cellular pathways.

KW - Adenosine Triphosphatases

KW - Arabidopsis

KW - Arabidopsis Proteins

KW - Catalytic Domain

KW - Chromatin Assembly and Disassembly

KW - Chromosomal Proteins, Non-Histone

KW - Gene Expression Profiling

KW - Gene Expression Regulation, Plant

KW - Gibberellins

KW - Molecular Sequence Annotation

KW - Mutation

KW - Phenotype

KW - Plant Growth Regulators

KW - Promoter Regions, Genetic

KW - Quantitative Trait, Heritable

KW - Signal Transduction

KW - Transcription Factors

KW - Triazoles

U2 - 10.1371/journal.pone.0058588

DO - 10.1371/journal.pone.0058588

M3 - Article

C2 - 23536800

SN - 1932-6203

VL - 8

SP - 1

EP - 12

JO - PLoS ONE

JF - PLoS ONE

IS - 3

M1 - e58588

ER -