Sugar-mediated regulation of hormone signaling is crucial for optimizing growth under normal conditions and ensuring survival during environmental stress.Previous studies have shown that sugar starvation in-duces the ...Sugar-mediated regulation of hormone signaling is crucial for optimizing growth under normal conditions and ensuring survival during environmental stress.Previous studies have shown that sugar starvation in-duces the degradation of BRASSINAZOLE RESISTANT 1(BZR1),the master transcription factor of the bras-sinosteroid(BR)signaling pathway,thereby inhibiting growth.However,the molecular mechanism linking sugar signaling to BZR1 degradation remains unknown.To identify proteins that mediate starvation-induced BZR1 degradation,we performed a quantitative proteomic analysis of the BZR1 interactome under starvation conditions and identified UBIQUITIN PROTEIN LIGASE 3(UPL3)as a sugar-regulated protein that promotes BZR1 degradation and regulates growth and survival in response to sugar availability.upl3 mu-tants showed increased BZR1 accumulation and larger seedling size compared to the wild type under sugar-limiting conditions,but not when grown on sugar-containing medium,which indicates that UPL3 me-diates BZR1 degradation and growth inhibition under sugar-limited conditions.Although upl3 mutations promoted growth under short-term starvation,they substantially reduced survival under long-term starva-tion.The enhanced growth phenotype of upl3 was also observed when target of rapamycin(TOR)was inactivated,but not when BR biosynthesis was blocked,suggesting that UPL3 acts downstream of sugar-TOR signaling to regulate BZR1 degradation.Furthermore,UPL3 protein levels increased post-transcriptionally in response to starvation and TOR inhibition,and decreased upon sugar treatment.Our study identifies UPL3 as a key molecular link between sugar signaling and BR signaling.We propose that sugar-TOR signaling inhibits UPL3 to promote BZR1 accumulation and growth,thereby optimizing plant growth and survival in response to sugar availability.展开更多
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...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.展开更多
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 regula...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.展开更多
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 p...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.展开更多
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 hy...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.展开更多
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 p...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.展开更多
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 B...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.展开更多
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 glu...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.展开更多
Stomata are epidermal pores that are essential for water evaporation and gas exchange in plants.Stomatal development is orchestrated by intrinsic developmental programs,hormonal controls,and environmental cues.The ste...Stomata are epidermal pores that are essential for water evaporation and gas exchange in plants.Stomatal development is orchestrated by intrinsic developmental programs,hormonal controls,and environmental cues.The steroid hormone brassinosteroid(BR)inhibits stomatal lineage progression by regulating BIN2 and BSL proteins in leaves.Notably,BR is known to promote stomatal development in hypocotyls as opposed to leaves;however,its molecular mechanism remains elusive.Here,we show that BR signaling has a dual regulatory role in controlling stomatal development in Arabidopsis hypocotyls.We found that brassinolide(BL;the most active BR)regulates stomatal development differently in a concentration-dependent manner.At low and moderate concentrations,BL promoted stomatal formation by upregulating the expression of SPEECHLESS(SPCH)and its target genes independently of BIN2 regulation.In contrast,high concentrations of BL and bikinin,which is a specific inhibitor of BIN2 and its homologs,significantly reduced stomatal formation.Genetic analyses revealed that BIN2 regulates stomatal development in hypocotyls through molecular mechanisms distinct from the regulatory mechanism of the cotyledons.In hypocotyls,BIN2 promoted stomatal development by inactivating BZR1,which suppresses the expression of SPCH and its target genes.Taken together,our results suggest that BR precisely coordinates the stomatal development of hypocotyls using an antagonistic control of SPCH expression via BZR1-dependent and BZR1-independent transcriptional regulation.展开更多
基金supported by grants from the National Institute of General Medical Sciences(R01GM066258 to Z.-Y.W.and S10OD030441 to S.-L.X.)the National Natural Science Foundation of China(31800239,http://www.nsfc.gov.cn)the China Scholarship Council(to Z.Z.).
文摘Sugar-mediated regulation of hormone signaling is crucial for optimizing growth under normal conditions and ensuring survival during environmental stress.Previous studies have shown that sugar starvation in-duces the degradation of BRASSINAZOLE RESISTANT 1(BZR1),the master transcription factor of the bras-sinosteroid(BR)signaling pathway,thereby inhibiting growth.However,the molecular mechanism linking sugar signaling to BZR1 degradation remains unknown.To identify proteins that mediate starvation-induced BZR1 degradation,we performed a quantitative proteomic analysis of the BZR1 interactome under starvation conditions and identified UBIQUITIN PROTEIN LIGASE 3(UPL3)as a sugar-regulated protein that promotes BZR1 degradation and regulates growth and survival in response to sugar availability.upl3 mu-tants showed increased BZR1 accumulation and larger seedling size compared to the wild type under sugar-limiting conditions,but not when grown on sugar-containing medium,which indicates that UPL3 me-diates BZR1 degradation and growth inhibition under sugar-limited conditions.Although upl3 mutations promoted growth under short-term starvation,they substantially reduced survival under long-term starva-tion.The enhanced growth phenotype of upl3 was also observed when target of rapamycin(TOR)was inactivated,but not when BR biosynthesis was blocked,suggesting that UPL3 acts downstream of sugar-TOR signaling to regulate BZR1 degradation.Furthermore,UPL3 protein levels increased post-transcriptionally in response to starvation and TOR inhibition,and decreased upon sugar treatment.Our study identifies UPL3 as a key molecular link between sugar signaling and BR signaling.We propose that sugar-TOR signaling inhibits UPL3 to promote BZR1 accumulation and growth,thereby optimizing plant growth and survival in response to sugar availability.
文摘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.
文摘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.
基金grants from the National Natural Science Foundation of China(91417313 to W.T.)the Department of Education of Hebei Province(LJRC015 to W.T.)the "One Hundred Talents Project"of Hebei Province(E2013100004 to Y.S.).
文摘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.
文摘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.
基金supported by grants from the National Natural Science Foundation of China(91935304)the Innovative Postdoctoral Research Initiative of Henan Province(to G.Q.)the National Science Foundation(EAGER grant 1464527 and grant IOS-1758994 to Z.Q.F.).
文摘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.
基金the National Natural Science Foundation of China(32070342 and 32270339)the Agri-X Interdisciplinary Fund of Shanghai Jiao Tong University(Agri-X20200204)+1 种基金the Bio-X Interdisciplinary Fund of Shanghai Jiao Tong University(20CX-04)the Scientific and Technological Innovation Funds of Shanghai Jiao Tong University(19X160020009).
文摘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.
基金supported by the National Science Foundation of China (31830078, 32172593, and 32202466)Zhejiang Provincial Ten-thousand Program for Leading Talents of Science and Technology Innovation (2018R52026)。
文摘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.
基金supported by the National Research Foundation of Korea(NRF)grant funded by the Korean government(Ministry of Science and ICT or Ministry of Education)(2021R1A2C1006617 and RS-2024-00407469 to T.-W.K.)supported by the Korea Basic Science Institute(National Research Facilities and Equipment Center)grant funded by the Ministry of Education(2023R1A6C101A009 to T.-K.P.)the research fund of Hanyang University(HY-202200000003024 to T.-K.P.)。
文摘Stomata are epidermal pores that are essential for water evaporation and gas exchange in plants.Stomatal development is orchestrated by intrinsic developmental programs,hormonal controls,and environmental cues.The steroid hormone brassinosteroid(BR)inhibits stomatal lineage progression by regulating BIN2 and BSL proteins in leaves.Notably,BR is known to promote stomatal development in hypocotyls as opposed to leaves;however,its molecular mechanism remains elusive.Here,we show that BR signaling has a dual regulatory role in controlling stomatal development in Arabidopsis hypocotyls.We found that brassinolide(BL;the most active BR)regulates stomatal development differently in a concentration-dependent manner.At low and moderate concentrations,BL promoted stomatal formation by upregulating the expression of SPEECHLESS(SPCH)and its target genes independently of BIN2 regulation.In contrast,high concentrations of BL and bikinin,which is a specific inhibitor of BIN2 and its homologs,significantly reduced stomatal formation.Genetic analyses revealed that BIN2 regulates stomatal development in hypocotyls through molecular mechanisms distinct from the regulatory mechanism of the cotyledons.In hypocotyls,BIN2 promoted stomatal development by inactivating BZR1,which suppresses the expression of SPCH and its target genes.Taken together,our results suggest that BR precisely coordinates the stomatal development of hypocotyls using an antagonistic control of SPCH expression via BZR1-dependent and BZR1-independent transcriptional regulation.
