Untargeted mutagenesis of brassinosteroid receptor SbBRI1 confers drought tolerance by altering phenylpropanoid metabolism in Sorghum bicolor

Summary Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this stud...

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Published inPlant biotechnology journal Vol. 22; no. 12; pp. 3406 - 3423
Main Authors Fontanet‐Manzaneque, Juan B., Laibach, Natalie, Herrero‐García, Iván, Coleto‐Alcudia, Veredas, Blasco‐Escámez, David, Zhang, Chen, Orduña, Luis, Alseekh, Saleh, Miller, Sara, Bjarnholt, Nanna, Fernie, Alisdair R., Matus, José Tomás, Caño‐Delgado, Ana I.
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons, Inc 01.12.2024
John Wiley and Sons Inc
Subjects
Abiotic stress
Adaptation
Arabidopsis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis - physiology
Biosynthesis
biotechnology
Brassinosteroids
Brassinosteroids - metabolism
BRI1
Cell death
Corn
DAP‐seq
DNA
DNA sequencing
Drought
Drought Resistance
drought tolerance
Droughts
Flavonoids
Gene Expression Regulation, Plant
Gene sequencing
Genetic engineering
Homeostasis
Kinases
lignin
Mutagenesis
Mutation - genetics
Phenylpropanoid
photosynthesis
Plant Proteins - genetics
Plant Proteins - metabolism
Plants (botany)
Proteins
radiation resistance
Receptors
Signal transduction
Sorghum
Sorghum - genetics
Sorghum - metabolism
Sorghum bicolor
Stress, Physiological - genetics
Transcription factors
water stress
Brassinosteroids
Sorghum bicolor
DAP‐seq
Drought
BRI1
Phenylpropanoid
Online AccessGet full text
ISSN1467-7644
1467-7652
1467-7652
DOI10.1111/pbi.14461

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Abstract Summary Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID‐INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP‐seq), we show that the sorghum BRI1‐EMS‐SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G‐box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1‐mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.
AbstractList Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID‐INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP‐seq), we show that the sorghum BRI1‐EMS‐SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G‐box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1‐mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.
Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID‐INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP‐seq), we show that the sorghum BRI1‐EMS‐SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G‐box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1‐mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.
Summary Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID‐INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP‐seq), we show that the sorghum BRI1‐EMS‐SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G‐box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1‐mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.
Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID-INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP-seq), we show that the sorghum BRI1-EMS-SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G-box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1-mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to abiotic stresses, particularly in the field of brassinosteroid (BR) signalling, has been the subject of extensive research. In this study, we unveil compelling insights indicating that the BRASSINOSTEROID-INSENSITIVE 1 (BRI1) receptor in Arabidopsis and Sorghum plays a critical role as a negative regulator of drought responses. Introducing untargeted mutation in the sorghum BRI1 receptor (SbBRI1) effectively enhances the plant's ability to withstand osmotic and drought stress. Through DNA Affinity Purification sequencing (DAP-seq), we show that the sorghum BRI1-EMS-SUPPRESSOR 1 (SbBES1) transcription factor, a downstream player of the BR signalling, binds to a conserved G-box binding motif, and it is responsible for regulating BR homeostasis, as its Arabidopsis ortholog AtBES1. We further characterized the drought tolerance of sorghum bri1 mutants and decipher SbBES1-mediated regulation of phenylpropanoid pathway. Our findings suggest that SbBRI1 signalling serves a dual purpose: under normal conditions, it regulates lignin biosynthesis by SbBES1, but during drought conditions, BES1 becomes less active, allowing the activation of the flavonoid pathway. This adaptive shift improves the photosynthetic rate and photoprotection, reinforcing crop adaptation to drought.
Author Zhang, Chen
Miller, Sara
Bjarnholt, Nanna
Caño‐Delgado, Ana I.
Laibach, Natalie
Alseekh, Saleh
Fernie, Alisdair R.
Herrero‐García, Iván
Coleto‐Alcudia, Veredas
Blasco‐Escámez, David
Matus, José Tomás
Fontanet‐Manzaneque, Juan B.
Orduña, Luis
AuthorAffiliation 5 Copenhagen Plant Science Center, Department of Plant and Environmental Sciences University of Copenhagen Frederiksberg Denmark
7 Present address: VIB‐UGent Center for Plant Systems Biology Ghente Belgium
4 Center of Plant Systems Biology and Biotechnology Plovdiv Bulgaria
6 Present address: Rhine‐Waal University of Applied Science, University of Copenhagen, Life Science Faculty Kleve Denmark
3 Max‐Planck‐Institute of Molecular Plant Physiology Potsdam‐Golm Germany
1 Department of Molecular Genetics Centre for Research in Agricultural Genomics (CRAG) CSIC‐IRTA‐UAB‐UB Barcelona Spain
2 Institute for Integrative Systems Biology (I2SysBio) Universitat de València‐CSIC Paterna Valencia Spain
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/39325724$$D View this record in MEDLINE/PubMed
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Copyright 2024 The Author(s). published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2024 The Author(s). Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
2024. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2024 The Author(s). published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
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– notice: 2024. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Issue 12
Keywords Brassinosteroids
Sorghum bicolor
DAP‐seq
Drought
BRI1
Phenylpropanoid
Language English
License Attribution-NonCommercial-NoDerivs
2024 The Author(s). Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
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Snippet Summary Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant...
Drought is a critical issue in modern agriculture; therefore, there is a need to create crops with drought resilience. The complexity of plant responses to...
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proquest
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 3406
SubjectTerms Abiotic stress
Adaptation
Arabidopsis
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis - physiology
Biosynthesis
biotechnology
Brassinosteroids
Brassinosteroids - metabolism
BRI1
Cell death
Corn
DAP‐seq
DNA
DNA sequencing
Drought
Drought Resistance
drought tolerance
Droughts
Flavonoids
Gene Expression Regulation, Plant
Gene sequencing
Genetic engineering
Homeostasis
Kinases
lignin
Mutagenesis
Mutation - genetics
Phenylpropanoid
photosynthesis
Plant Proteins - genetics
Plant Proteins - metabolism
Plants (botany)
Proteins
radiation resistance
Receptors
Signal transduction
Sorghum
Sorghum - genetics
Sorghum - metabolism
Sorghum bicolor
Stress, Physiological - genetics
Transcription factors
water stress
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Title Untargeted mutagenesis of brassinosteroid receptor SbBRI1 confers drought tolerance by altering phenylpropanoid metabolism in Sorghum bicolor
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpbi.14461
https://www.ncbi.nlm.nih.gov/pubmed/39325724
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Volume 22
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