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Brassinosteroids fine-tune secondary and primary sulfur metabolism through bzr1-mediated transcriptional regulation

Journal of Integrative Plant Biology 2023年第5期65卷 1153-1169页

作者： Mengyu Wang Congxi Cai Yubo Li Han Tao Fanliang Meng Bo Sun Huiying Miao Qiaomei Wang Department of Horticulture Key Laboratory of Horticultural Plant GrowthDevelopment and Quality improvementMinistry of AgricultureZhejiang UniversityHangzhou 310058China School of Horticulture and Landscape Architecture Yangzhou UniversityYangzhou 221116China Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province Zhejiang Academy of Agricultural SciencesHangzhou 310021China College of Horticulture Sichuan Agricultural UniversityChengdu 611130China

For adaptation to ever-changing environments,plants have evolved elaborate metabolic systems coupled to a regulatory network for optimal growth and defense. Regulation of plant secondary metabolic pathways such as glucosinolates(GSLs) by defense phytohormones in response to different stresses and nutrient deficiency has been intensively investigated, while how growth-promoting hormone balances plant secondary and primary metabolism has been largely unexplored. Here, we found that growth-promoting hormone brassinosteroid(BR) inhibits GSLs accumulation while enhancing biosynthesis of primary sulfur metabolites, including cysteine(Cys) and glutathione(GSH) both in Arabidopsis and Brassica crops, fine-tuning secondary and primary sulfur metabolism to promote plant growth. Furthermore, we demonstrate that of BRASSINAZOLE RESISTANT 1(bzr1), the central component of BR signaling, exerts distinct transcriptional inhibition regulation on indolic and aliphatic GSL via direct MYB51 dependent repression of indolic GSL biosynthesis, while exerting partial MYB29 dependent repression of aliphatic GSL biosynthesis. Additionally, bzr1 directly activates the transcription of APR1 and APR2 which encodes rate-limiting enzyme adenosine 5′-phosphosulfate reductases in the primary sulfur metabolic pathway.In summary, our findings indicate that BR inhibits the biosynthesis of GSLs to prioritize sulfur usage for primary metabolites under normal growth conditions.These findings expand our understanding of BR promoting plant growth from a metabolism perspective.

关键词： brassinosteroids bzr1 glucosinolates plant growth primary sulfur metabolites secondary sulfur metabolites

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Brassinosteroid signaling regulates phosphate starvation-induced malate secretion in plants

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Journal of Integrative Plant Biology 2023年第5期65卷 1099-1112页

作者： Tongtong Liu Suren Deng Cheng Zhang Xu Yang Lei Shi Fangsen Xu Sheliang Wang Chuang Wang Microelement Research Center College of Resources&EnvironmentHuazhong Agricultural UniversityWuhan430070 China Key Laboratory of Arable Land Conservation(Middle and Lower Reaches of Yangtze River) Ministry of AgricultureHuazhong Agricultural UniversityWuhan430070 China

Inorganic phosphate(Pi)is often limited in soils due to precipitation with iron(Fe)and aluminum(Al).To scavenge heterogeneously distributed phosphorus(P)resources,plants have evolved a local Pi signaling pathway that induces malate secretion to solubilize the occluded Fe-P or Al-P oxides.In this study,we show that Pi limitation impaired brassinosteroid signaling and downregulated BRASSINAZOLE-RESISTANT 1(bzr1)expression in Arabidopsis thaliana.Exogenous 2,4-epibrassinolide treatment or constitutive activation of bzr1(in the bzr1-D mutant)significantly reduced primary root growth inhibition under Pi-starvation conditions by downregulating ALUMINUM-ACTIVATED MALATE TRANSPORTER 1(ALMT1)expression and malate secretion.Furthermore,At bzr1 competitively suppressed the activator effect of SENSITIVITY TO PROTON RHIZOTOXICITY 1(STOP1)on ALMT1 expression and malate secretion in Nicotiana benthamiana leaves and Arabidopsis.The ratio of nuclear-localized STOP1 and bzr1 determined ALMT1 expression and malate secretion in Arabidopsis.In addition,bzr1-inhibited malate secretion is conserved in rice(Oryza sativa).Our findings provide insight into plant mechanisms for optimizing the secretion of malate,an important carbon resource,to adapt to Pi-deficiency stress.

关键词： ALMT1 brassinosteroid signaling bzr1 malate phosphate deficiency STOP1

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Brassinosteroid signaling positively regulates abscisic acid biosynthesis in response to chilling stress in tomato

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Journal of Integrative Plant Biology 2023年第1期65卷 10-24页

作者： Shengmin An Yue Liu Kangqi Sang Ting Wang Jingquan Yu Yanhong Zhou Xiaojian Xia Department of Horticulture Zhejiang University Hangzhou 310058 China Hainan Institute Zhejiang University Sanya 572025 China Key Laboratory of Horticultural Plants Growth Development and Quality ImprovementAgricultural Ministry of ChinaHangzhou 310058 China

Brassinosteroids(BRs)and abscisic acid(ABA)are essential regulators of plant growth and stress tolerance.Although the antagonistic interaction of BRs and ABA is proposed to ensure the balance between growth and defense in model plants,the crosstalk between BRs and ABA in response to chilling in tomato(Solanum lycopersicum),a warmclimate horticultural crop,is unclear.Here,we determined that overexpression of the BR biosynthesis gene DWARF(DWF)or the key BR signaling gene BRASSINAZOLE-RESISTANT1(bzr1)increases ABA levels in response to chilling stress via positively regulating the expression of the ABA biosynthesis gene 9-CIS-EPOXYCAROTENOID DIOXYGENASE1(NCED1).BR-induced chilling tolerance was mostly dependent on ABA biosynthesis.Chilling stress or high BR levels decreased the abundance of BRASSINOSTEROID-INSENSITIVE2(BIN2),a negative regulator of BR signaling.Moreover,we observed that chilling stress increases BR levels and results in the accumulation of bzr1.BIN2negatively regulated both the accumulation of bzr1protein and chilling tolerance by suppressing ABA biosynthesis.Our results demonstrate that BR signaling positively regulates chilling tolerance via ABA biosynthesis in tomato.The study has implications in production of warm-climate crops in horticulture.

关键词： ABA BIN2 bzr1 chilling stress NCED

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Vacuolar H^(+)-ATPase and bzr1 form a feedback loop to regulate the homeostasis of BR signaling inArabidopsis

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Molecular Plant 2023年第12期16卷 1976-1989页

作者： Yu-Tong Jiang Lu-Han Yang Ji-Xuan Zheng Xian-Chen Geng Yu-Xuan Bai Yu-Chen Wang Hong-Wei Xue Wen-Hui Lin School of Life Sciences and Biotechnology The Joint International Research Laboratory of Metabolic&Developmental SciencesShanghai Jiao Tong UniversityShanghai 200240China Shanghai Collaborative Innovation Center of Agri-Seeds Joint Center for Single Cell BiologyShanghai 200240China School of Agricuture and Biology Shanghai Jiao Tong UniversityShanghai 200240China Zhiyuan College Shanghai Jiao Tong UniversityShanghai 200240China

Brassinosteroid(BR)is a vital plant hormone that regulates plant growth anddevelopment.BRASSINAZOLE RESISTANT1(bzr1)is a key transcription factor in BR signaling,and its nucleocytoplasmic localization is crucial for BR signaling.However,the mechanisms that regulate bzr1 nucleocytoplasmic distribution and thus the homeostasis of BR signaling remain largely unclear.The vacuole is the largest organelle in mature plantcells and plays a key role in maintenance of cell ular pH,storage of intracellular substances,and transport ofions.In this study,weuncovered anovel mechanismof BR signaling homeostasis regulatedbythe vacuolar H+-ATPase(V-ATPase)and bzr1 feedback loop.Our results revealed that the vha-a2 vha-a3 mutant(vha2,lacking V-ATPase activity)exhibits enhanced BR signaling with increased total amount of bzr1,nuclearlocalized bzr1,and the ratio of bzr1/phosphorylated bzr1 in the nucleus.Further biochemical assays revealed that VHA-a2 and VHA-a3 of V-ATPase interact with the bzr1 protein through a domain that is conserved across multiple species.VHA-a2 and VHA-a3 negatively regulate BR signaling by interacting with bzr1 and promoting its retention in the tonoplast.Interestingly,a series of molecular analyses demonstrated that nuclear-localized bzr1 could bind directlyto specific motifs in the promoters of VHA-a2 andVHAa3topromote their expression.Taken together,these results suggest that V-ATPase and bzr1 mayforma feedback regulatory loop to maintain thehomeostasis of BR signaling in Arabidopsis,providing new insights into vacuole-mediated regulation of hormone signaling.

关键词： BR bzr1 vacuole V-ATPase tonoplast

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bzr1 Family Transcription Factors Function Redundantly and Indispensably in BR Signaling but Exhibit BRI1-Independent Function in Regulating Anther Development in Arabidopsis

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Molecular Plant 2019年第10期12卷 1408-1415页

作者： Lian-Ge Chen Zhihua Gao Zhiying Zhao Xinye Liu Yongpeng Li Yuxiang Zhang Xigang Liu Yu Sun Wenqiang Tang Ministry of Education Key Laboratory of Molecular and Cellular Biology Hebei Key Laboratory of Molecular and Cellular BiologyCollege of Life SciencesHebei Normal UniversityShijiazhuang 050024China Hebei Collaboration Innovation Center for Cell Signaling Shijiazhuang 050024China State Key Laboratory of Plant Cell and Chromosome Engineering Center for Agricultural Resources ResearchInstitute of Genetics and Developmental Biologythe Innovative Academy of Seed DesignChinese Academy of SciencesShijiazhuang 050021China

BRASSINAZOLE-RESISTANT 1 family proteins(bzrs)are central transcription factors that govern brassinosteroid(BR)-regulated gene expression and plant growth.However,it is unclear whether there exists a bzr-independent pathway that mediates BR signaling.In this study,we found that disruption of all bzrs in Arabidopsis generated a hextuple mutant(bzr-h)displaying vegetative growth phenotypes that were almost identical to those of the null mutant of three BR receptors,bri1brl1brl3(bri-t).By RNA sequencing,we found that global gene expression in bzr-h was unaffected by 2 h of BR treatment.The anthers of bzr-h plants were loculeless,but a similar phenotype was not observed in bri-t,suggesting that bzrs have a BR signaling-independent regulatory role in anther development.By real-time PCR and in situ hybridization,we found that the expression of SPOROCYTELESS(SPL),which encodes a transcription factor essential for anther locule development,was barely detectable in bzr-h,suggesting that bzrs regulate locule development by affecting SPL expression.Our findings reveal that bzrs are indispensable transcription factors required for both BR signaling and anther locule development,providing new insight into the molecular mechanisms underlying the microsporogenesis in Arabidopsis.

关键词： brassinosteroid bzr1 anther development SPL gene expression

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bzr1 Positively Regulates Freezing Tolerance via CBF-Dependent and CBF-Independent Pathways in Arabidopsis

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Molecular Plant 2017年第4期10卷 545-559页

作者： Hui Li Keyi Ye Yiting Shi Jinkui Cheng Xiaoyan Zhang Shuhua Yang State Key Laboratory of Plant Physiology and Biochemistry College of Biological Sciences China Agricultural University Beijing 100193 China These authors contributed equally to this article.

Cold stress is a major environmental factor that adversely affects plant growth and development. The C-repeat binding factor/DRE binding factor 1 （CBF/DREB1） transcriptional regulatory cascade has been shown to play important roles in plant response to cold. Here we demonstrate that two key components of brassinosteroid （BR） signaling modulate freezing tolerance of Arabidopsis plants. The loss-of-function mutant of the GSK3-1ike kinases involved in BR signaling, bin2-3 bill bil2, showed increased freezing tolerance, whereas overexpression of BIN2 resulted in hypersensitivity to freezing stress under both non-acclimated and acclimated conditions. By contrast, gain-of-function mutants of the transcription factors bzr1 and BES1 displayed enhanced freezing tolerance, and consistently cold treatment could induce the accumulation of dephosphorylated bzr1. Biochemical and genetic analyses showed that bzr1 acts upstream of CBF1 and CBF2 to directly regulate their expression. Moreover, we found that bzr1 also regulated other COR genes uncoupled with CBFs, such as WKRY6, PYL6, SOCl, JMT, and SAG21, to modulate plant response to cold stress. Consistently, wrky6 mutants showed decreased freezing tolerance. Taken together, our results indicate that bzr1 positively modulates plant freezing tolerance through CBF-dependent and CBF-independent pathways.

关键词： BIN2 bzr1 freezing tolerance CBF Arabidopsis

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bzr1 Interacts with HY5 to Mediate Brassinosteroid- and Light-Regulated Cotyledon Opening in Arabidopsis in Darkness

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Molecular Plant 2016年第1期9卷 113-125页

作者： Qian-Feng Li Jun-Xian He School of Life Sciences and State Key Laboratory of Agrobiotechnology The Chinese University of Hong Kong 186 Science Center (South) Shatin New TerritoriesHong Kong Special Administration Region China Key Laboratory of Plant Functional Genomics of Ministry of Education and Key Laboratory of Crop Genetics and Physiology Agricultural College YangzhouUniversity Jiangsu 225009 China

Light and brassinosteroid （BR） are two central stimuli that regulate plant photomorphogenesis. Although previous phenotypic and physiological studies have implied possible interactions between BR and light in regulating photomorphogenesis, the underlying molecular mechanism（s） remain largely unknown. In the present study, we identified a physical connection between the BR and light signaling pathways, which was mediated by the BR-regulated transcription factor bzr1 and light-regulated transcription factor HY5 in Arabidopsis thaliana. Genetic evidence showed that the gain-of-function bzrl-lD mutant in the BR signaling pathway and loss-of-function hy5-215 mutant in the light signaling pathway exhibited closed cotyledons under BR-deficient and dark-grown conditions and both bzrl-lD and hy5-215 mutants were able to suppress the cotyledon opening phenotype of the BR-insensitive mutants bril-5 and bin2-1. Biochemical studies demonstrated that bzr1 interacts with HY5 both in vitro and in vivo and ectopic expression of HY5 considerably reduces the accumulation of bzr1 protein. In addition, HY5 specifically interacts with the dephosphorylated form of bzr1 and attenuates bzrI＇s transcriptional activity in regulating its target genes related to cotyledon opening. Our study provides a molecular framework for coordination of BR and light signals in regulating cotyledon opening, an important process in photomor- phogenesis in plants.

关键词： photomorphogenesis brassinosteroid light HY5 bzr1 Arabidopsis thaliana

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The Blue-Light Receptor CRY1 Interacts with bzr1 and BIN2 to Modulate the Phosphorylation and Nuclear Function of bzr1 in Repressing BR Signaling in Arabidopsis

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Molecular Plant 2019年第5期12卷 689-703页

作者： Guanhua He Jie Liu Huixue Dong Jiaqiang Sun National Key Facility for Crop Gene Resources and Genetic Improvement Institute of Crop SciencesChinese Academy of Agricultural SciencesBeijing 100081China

The blue-light receptor cryptochrome 1(CRY1)primarily mediates blue-light inhibition of hypocotyl elongation in Arabidopsis.However,the underlying mechanisms remain largely elusive.We report here that CRY1 inhibits hypocotyl elongation by repressing brassinosteroid(BR)signaling.A genetic interaction assay reveals the negative regulatory effect of CRY1 on the function of bzr1,a core transcription factor in the BR signaling pathway.We demonstrated that CRY1 interacts with the DNA-binding domain of bzr1 to interfere with the DNA-binding ability of bzr1,and represses its transcriptional activity.Furthermore,we found that CRY1 promotes the phosphorylation of bzr1 and inhibits the nuclear accumulation of bzr1.Interestingly,we discovered that CRY1 interacts with the GSK3-like kinase BIN2 and enhances the interaction of BIN2 and bzr1 in a light-dependent manner.Our findings revealed that CRY1 negatively regulates the function of bzr1 through at least two mechanisms:interfering with the DNA-binding ability of bzr1 and promoting the phosphorylation of bzr1.Therefore,we uncover a novel CRY1-BIN2-bzr1 regulatory module that mediates crosstalk between blue light and BR signaling to coordinate plant growth in Arabidopsis.

关键词： brassinosteroid BIN2 bzr1 cryptochrome 1

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The bzr1-EDS1 module regulates plant growth-defense coordination

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Molecular Plant 2021年第12期14卷 2072-2087页

作者： Guang Qi Huan Chen Dian Wang Hongyuan Zheng Xianfeng Tang Zhengzheng Guo Jiayu Cheng Jian Chen Yiping Wang Ming-yi Bai Fengquan Liu Daowen Wang Zheng Qing Fu State Key Laboratory of Wheat and Maize Crop Science College of Agronomyand Center for Crop Genome EngineeringHenan Agricultural UniversityZhengzhou 450002China Department of Biological Sciences University of South CarolinaColumbiaSC 29208USA Institute of Plant Protection Jiangsu Academy of Agricultural SciencesNanjing210014China College of Agronomy Qingdao Agricultural UniversityQingdao 266109China Qingdao Institute of BioEnergy and Bioprocess Technology Chinese Academy of SciencesQingdao 266109China Key Laboratory of Plant Development and Environment Adaptation Biology Ministry of EducationSchool of Life SciencesShandong University266237 QingdaoChina

Plants have developed sophisticated strategies to coordinate growth and immunity,but our understanding of the underlying mechanism remains limited.In this study,we identified a novel molecular module that reg-ulates plant growth and defense in both compatible and incompatible infections.This module consisted of bzr1,a key transcription factor in brassinosteroid(BR)signaling,and EDS1,an essential positive regulator of plant innate immunity.We found that EDS1 interacts with bzr1 and suppresses its transcriptional activ-ities.Consistently,upregulation of EDS1 function by a virulent Pseudomonas syringae strain or salicylic acid treatment inhibited bzr1-regulated expression of BR-responsive genes and BR-promoted growth.Furthermore,we showed that the cytoplasmic fraction of bzr1 positively regulates effector-triggered im-munity(ETI)controlled by the TIR-NB-LRR protein RPS4,which is attenuated by bzr1's nuclear transloca-tion.Mechanistically,cytoplasmic bzr1 facilitated AvrRps4-triggered dissociation of EDS1 and RPS4 by binding to EDS1,thus leading to efficient activation of RPS4-controlled ETI.Notably,transgenic expression of a mutant bzr1 that accumulates exclusively in the cytoplasm improved pathogen resistance without compromising plant growth.Collectively,these results shed new light on plant growth-defense coordina-tion and reveal a previously unknown function for the cytoplasmic fraction of bzr1.The bzr1-EDS1 mod-ule may be harnessed for the simultaneous improvement of crop productivity and pathogen resistance.

关键词： brassinosteroid bzr1 salicylic acid EDS1 basal resistance effector-triggered immunity TIR-NB-LRR resistance protein RPS4

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A PP2C-1 Allele Underlying a Quantitative Trait Locus Enhances Soybean l O0-Seed Weight

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Molecular Plant 2017年第5期10卷 670-684页

作者： Xiang Lu Qing Xiong Tong Cheng Qing-Tian Li Xin-Lei Liu Ying-Dong Bi Wei Li Wan-Ke Zhang Biao Ma Yong-Cai Lai Wei-Guang Du Wei-Qun Man Shou-Yi Chen Jin-Song Zhang State Key Lab of Plant Genomics Institute of Genetics and Developmental Biology Chinese Academy of Sciences Beijing 100101 China University of Chinese Academy of Sciences Beijing 100049 China Institute of Soybean Research Heilongjiang Provincial Academy of Agricultural Sciences Harbin 150086 China Institute of Farming and Cultivation Heilongjiang Provincial Academy of Agricultural Sciences Harbin 150086 China These authors contributed equally to this article

Cultivated soybeans may lose some useful genetic loci during domestication. Introgression of genes from wild soybeans could broaden the genetic background and improve soybean agronomic traits. In this study, through whole-genome sequencing of a recombinant inbred line population derived from a cross between a wild soybean ZYD7 and a cultivated soybean HN44, and mapping of quantitative trait loci for seed weight, we discovered that a phosphatase 2C-1 （PP2C-1） allele from wild soybean ZYD7 contributes to the increase in seed weight/size. PP2C-1 may achieve this function by enhancing cell size of integument and activating a subset of seed trait-related genes. We found that PP2C-1 is associ- ated with Gmbzr1, a soybean ortholog of Arabidopsis bzr1, one of key transcription factors in brassi- nosteroid （BR） signaling, and facilitate accumulation of dephosphorylated Gmbzr1. In contrast, the PP2C-2 allele with variations of a few amino acids at the N-terminus did not exhibit this function. More- over, we showed that Gmbzr1 could promote seed weight/size in transgenic plants. Through analysis of cultivated soybean accessions, we found that 40% of the examined accessions do not have the PP2C-1 allele, suggesting that these accessions can be improved by introduction of this allele. Taken together, our study identifies an elite allele PP2C-1, which can enhance seed weight and/or size in soybean, and pinpoints that manipulation of this allele by molecular-assisted breeding may increase production in soybean and other legumes/crops.

关键词： soybean lO0-seed weight PP2C-1 bzr1

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