Nat Commun , IF:12.121 , 2019 May , V10 (1) : P2378 doi: 10.1038/s41467-019-10331-9
Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen.
Molecular Plant Nutrition, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany.; Heterosis, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany.; Molecular Plant Nutrition, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany. vonwiren@ipk-gatersleben.de.
Developmental plasticity of root system architecture is crucial for plant performance in nutrient-poor soils. Roots of plants grown under mild nitrogen (N) deficiency show a foraging response characterized by increased root length but mechanisms underlying this developmental plasticity are still elusive. By employing natural variation in Arabidopsis accessions, we show that the brassinosteroid (BR) signaling kinase BSK3 modulates root elongation under mild N deficiency. In particular, a proline to leucine substitution in the predicted kinase domain of BSK3 enhances BR sensitivity and signaling to increase the extent of root elongation. We further show that low N specifically upregulates transcript levels of the BR co-receptor BAK1 to activate BR signaling and stimulate root elongation. Altogether, our results uncover a role of BR signaling in root elongation under low N. The BSK3 alleles identified here provide targets for improving root growth of crops growing under limited N conditions.
PMID: 31147541
Mol Plant , IF:12.084 , 2019 May , V12 (5) : P689-703 doi: 10.1016/j.molp.2019.02.001
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.
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.; National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China. Electronic address: sunjiaqiang@caas.cn.
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.
PMID: 30763615
Plant Cell , IF:9.618 , 2019 May , V31 (5) : P1077-1093 doi: 10.1105/tpc.18.00836
Rice qGL3/OsPPKL1 Functions with the GSK3/SHAGGY-Like Kinase OsGSK3 to Modulate Brassinosteroid Signaling.
State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Agriculture, Nanjing Agricultural University, Nanjing 210095, China.; College of Agronomy, Qingdao Agricultural University, Qingdao 266109, China.; College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China.; State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Agriculture, Nanjing Agricultural University, Nanjing 210095, China huangji@njau.edu.cn.
Brassinosteroids (BRs) are steroid hormones that play essential roles in plant growth and development. We previously cloned qGL3, a major quantitative trait locus regulating grain length in rice (Oryza sativa). The O. sativa japonica var N411 has extra-large grains compared with the O. sativa indica var 9311, and the recessive qgl3 allele from N411 contributes positively to grain length. qGL3 encodes a putative protein phosphatase with Kelch-like repeat domains, an ortholog of Arabidopsis (Arabidopsis thaliana) brassinosteroid-insensitive1 SUPPRESSOR1 (BSU1). BSU1 positively regulates BR signaling, while overexpression of qGL3 induced BR loss-of-function phenotypes. Both qGL3(N411) and qGL3(9311) physically interact with the rice glycogen synthase kinase 3 (GSK3)/SHAGGY-like kinase 3 (OsGSK3), an ortholog of Arabidopsis BR INSENSITIVE2 (BIN2). qGL3(9311) dephosphorylates OsGSK3, but qGL3(N411) lacks this activity. Knocking out OsGSK3 enhances BR signaling and induces nuclear localization of O. sativa BRASSINAZOLE RESISTANT1 (OsBZR1). Unlike the dephosphorylation of BIN2 (which leads to protein degradation) in Arabidopsis, qGL3 dephosphorylates and stabilizes OsGSK3 in rice. These results demonstrate that qGL3 suppresses BR signaling by regulating the phosphorylation and stability of OsGSK3, which modulates OsBZR1 phosphorylation and subcellular distribution. Our study clarifies the role of qGL3 in the regulation of grain length and provides insight into BR signaling, including the differences between rice and Arabidopsis.
PMID: 30923230
Curr Biol , IF:9.601 , 2019 May , V29 (10) : P1669-1676.e4 doi: 10.1016/j.cub.2019.03.042
Soil Salinity Limits Plant Shade Avoidance.
Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Kruytgebouw, Padualaan 8, 3584CH, Utrecht, the Netherlands; Centro Nacional de Biotecnologia, CSIC, Calle Darwin 3, Madrid 28049, Spain.; Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Kruytgebouw, Padualaan 8, 3584CH, Utrecht, the Netherlands.; School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol BS8 1TQ, UK.; Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1098XH Amsterdam, the Netherlands.; Centro Nacional de Biotecnologia, CSIC, Calle Darwin 3, Madrid 28049, Spain.; Laboratory of Plant Physiology, Wageningen University and Research, Radix Building, Wageningen 6700 AA, the Netherlands.; Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Kruytgebouw, Padualaan 8, 3584CH, Utrecht, the Netherlands. Electronic address: r.pierik@uu.nl.
Global food production is set to keep increasing despite a predicted decrease in total arable land [1]. To achieve higher production, denser planting will be required on increasingly degraded soils. When grown in dense stands, crops elongate and raise their leaves in an effort to reach sunlight, a process termed shade avoidance [2]. Shade is perceived by a reduction in the ratio of red (R) to far-red (FR) light and results in the stabilization of a class of transcription factors known as PHYTOCHROME INTERACTING FACTORS (PIFs) [3, 4]. PIFs activate the expression of auxin biosynthesis genes [4, 5] and enhance auxin sensitivity [6], which promotes cell-wall loosening and drives elongation growth. Despite our molecular understanding of shade-induced growth, little is known about how this developmental program is integrated with other environmental factors. Here, we demonstrate that low levels of NaCl in soil strongly impair the ability of plants to respond to shade. This block is dependent upon abscisic acid (ABA) signaling and the canonical ABA signaling pathway. Low R:FR light enhances brassinosteroid (BR) signaling through BRASSINOSTEROID SIGNALING KINASE 5 (BSK5) and leads to the activation of BRI1 EMS SUPPRESSOR 1 (BES1). ABA inhibits BSK5 upregulation and interferes with GSK3-like kinase inactivation by the BR pathway, thus leading to a suppression of BES1:PIF function. By demonstrating a link between light, ABA-, and BR-signaling pathways, this study provides an important step forward in our understanding of how multiple environmental cues are integrated into plant development.
PMID: 31056387
Proc Natl Acad Sci U S A , IF:9.412 , 2019 May , V116 (21) : P10563-10567 doi: 10.1073/pnas.1821445116
beta-Cyclocitral is a conserved root growth regulator.
Department of Biology, Duke University, Durham, NC 27708.; Howard Hughes Medical Institute, Duke University, Durham, NC 27708.; Department of Plant Biology, Carnegie Institute of Science, Stanford, CA 94305.; Biological and Environmental Sciences and Engineering Division, The Bioactives Lab, King Abdullah University of Science and Technology, 23955-6900 Thuwal, Saudi Arabia.; Department of Biology, Stanford University, Palo Alto, CA 94305.; Department of Biology, Duke University, Durham, NC 27708; philip.benfey@duke.edu.
Natural compounds capable of increasing root depth and branching are desirable tools for enhancing stress tolerance in crops. We devised a sensitized screen to identify natural metabolites capable of regulating root traits in Arabidopsis beta-Cyclocitral, an endogenous root compound, was found to promote cell divisions in root meristems and stimulate lateral root branching. beta-Cyclocitral rescued meristematic cell divisions in ccd1ccd4 biosynthesis mutants, and beta-cyclocitral-driven root growth was found to be independent of auxin, brassinosteroid, and reactive oxygen species signaling pathways. beta-Cyclocitral had a conserved effect on root growth in tomato and rice and generated significantly more compact crown root systems in rice. Moreover, beta-cyclocitral treatment enhanced plant vigor in rice plants exposed to salt-contaminated soil. These results indicate that beta-cyclocitral is a broadly effective root growth promoter in both monocots and eudicots and could be a valuable tool to enhance crop vigor under environmental stress.
PMID: 31068462
New Phytol , IF:8.512 , 2019 May , V222 (3) : P1405-1419 doi: 10.1111/nph.15709
Identification of critical cysteine sites in brassinosteroid-insensitive 1 and novel signaling regulators using a transient expression system.
State Key Laboratory of Plant Genomics, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, Hebei, 050021, China.; University of Chinese Academy of Sciences, Beijing, 100049, China.; Key Laboratory for Protein Sciences of Ministry of Education, School of Life Sciences, Tsinghua University, Beijing, 100084, China.
The plant hormones brassinosteroids (BRs) modulate plant growth and development. Cysteine (Cys) residues located in the extracellular domain of a protein are of importance for protein structure by forming disulfide bonds. To date, the systematic study of the functional significance of Cys residues in BR-insensitive 1 (BRI1) is still lacking. We used brassinolide-induced exogenous bri1-EMS-Suppressor 1 (BES1) dephosphorylation in Arabidopsis thaliana protoplasts as a readout, took advantage of the dramatic decrease of BRI1 protein levels during protoplast isolation, and of the strong phosphorylation of BES1 by BR-insensitive 2 (BIN2) in protoplasts, and developed a protoplast transient system to identify critical Cys sites in BRI1. Using this system, we identified a set of critical Cys sites in BRI1, as substitution of these Cys residues with alanine residues greatly compromised the function of BRI1. Moreover, we identified two negative regulators of BR signaling, pattern-triggered immunity compromised RLCK1 (PCRK1) and PCRK2, that were previously known to positively regulate innate immunity signaling. This work not only provides insight into the functional importance of critical Cys residues in stabilizing the superhelical conformation of BRI1-leucine-rich-repeat, but also reveals that PCRK1/2 can inversely modulate BR and plant immune signaling pathways.
PMID: 30685894
Plant Physiol , IF:6.902 , 2019 May , V180 (1) : P18-19 doi: 10.1104/pp.19.00314
BRacing for Water Stress: Brassinosteroid Signaling Promotes Drought Survival in Wheat.
PMID: 31053677
Plant Physiol , IF:6.902 , 2019 May , V180 (1) : P605-620 doi: 10.1104/pp.19.00100
BES/BZR Transcription Factor TaBZR2 Positively Regulates Drought Responses by Activation of TaGST1.
Institute of Crop Science, Chinese Academy of Agricultural Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing 100081, China.; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China.; College of Plant Protection/College of Agronomy, Northwest A&F University, Yangling, Shaanxi 712100, China.; Institute of Genetics and Physiology, Hebei Academy of Agriculture and Forestry Sciences/Plant Genetic Engineering Center of Hebei Province, Shijiazhuang, Hebei 050051, China.; Institute of Crop Science, Chinese Academy of Agricultural Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Beijing 100081, China xuzhaoshi@caas.cn.
BRI1-EMS suppressor (BES)/brassinazole-resistant (BZR) family transcription factors are involved in a variety of physiological processes, but the biological functions of some BES/BZR transcription factors remain unknown; moreover, it is not clear if any of these proteins function in the regulation of plant stress responses. Here, wheat (Triticum aestivum) brassinazole-resistant 2 (TaBZR2)-overexpressing plants exhibited drought tolerant phenotypes, whereas downregulation of TaBZR2 in wheat by RNA interference resulted in elevated drought sensitivity. electrophoretic mobility shift assay and luciferase reporter analysis illustrate that TaBZR2 directly interacts with the gene promoter to activate the expression of T. aestivum glutathione s-transferase-1 (TaGST1), which functions positively in scavenging drought-induced superoxide anions (O2 (-)). Moreover, TaBZR2 acts as a positive regulator in brassinosteroid (BR) signaling. Exogenous BR treatment enhanced TaBZR2-mediated O2 (-) scavenging and antioxidant enzyme gene expression. Taken together, we demonstrate that a BES/BZR family transcription factor, TaBZR2, functions positively in drought responses by activating TaGST1 and mediates the crosstalk between BR and drought signaling pathways. Our results thus provide new insights into the mechanisms underlying how BES/BZR family transcription factors contribute to drought tolerance in wheat.
PMID: 30842265
Plant Physiol , IF:6.902 , 2019 May , V180 (1) : P543-558 doi: 10.1104/pp.18.01503
Proteolytic Processing of SERK3/BAK1 Regulates Plant Immunity, Development, and Cell Death.
Department of Biochemistry and Biophysics, and Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, Texas 77843.; Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, 200234 China.; Department of Plant Pathology and Microbiology, and Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, Texas 77843.; Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium.; Center for Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium.; College of Horticulture, Shandong Agricultural University, Tai'an, Shandong, 271018 China.; Department of Plant Pathology and Microbiology, and Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, Texas 77843 lshan@tamu.edu.
Plants have evolved many receptor-like kinases (RLKs) to sense extrinsic and intrinsic cues. The signaling pathways mediated by multiple Leucine-rich repeat (LRR) RLK (LRR-RLK) receptors require ligand-induced receptor-coreceptor heterodimerization and transphosphorylation with BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1)/SOMATIC EMBRYOGENESIS RECEPTOR KINASES family LRR-RLKs. Here we reveal an additional layer of regulation of BAK1 via a Ca(2+)-dependent proteolytic cleavage process that is conserved in Arabidopsis (Arabidopsis thaliana), Nicotiana benthamiana, and Saccharomyces cerevisiae The proteolytic cleavage of BAK1 is intrinsically regulated in response to developmental cues and immune stimulation. The surface-exposed Asp (D(287)) residue of BAK1 is critical for its proteolytic cleavage and plays an essential role in BAK1-regulated plant immunity, growth hormone brassinosteroid-mediated responses, and cell death containment. BAK1(D287A) mutation impairs BAK1 phosphorylation on its substrate BOTRYTIS-INDUCED KINASE1 (BIK1), and its plasma membrane localization. Intriguingly, it aggravates BAK1 overexpression-triggered cell death independent of BIK1, suggesting that maintaining homeostasis of BAK1 through a proteolytic process is crucial to control plant growth and immunity. Our data reveal that in addition to layered transphosphorylation in the receptor complexes, the proteolytic cleavage is an important regulatory process for the proper functions of the shared coreceptor BAK1 in diverse cellular signaling pathways.
PMID: 30782965
Plant Physiol , IF:6.902 , 2019 May , V180 (1) : P571-581 doi: 10.1104/pp.18.01143
AVR2 Targets BSL Family Members, Which Act as Susceptibility Factors to Suppress Host Immunity.
Division of Plant Science, School of Life Science, University of Dundee (at JHI), Invergowrie, Dundee DD2 5DA, United Kingdom.; Key Laboratory of Horticultural Plant Biology (HZAU), Ministry of Education, Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture, Huazhong Agricultural University, Wuhan, Hubei 430070, China.; Cell and Molecular Science, James Hutton Institute, Invergowrie, Dundee DD2 5DA, United Kingdom.; Department of Biochemistry, Centre for Plant Molecular Biology, Eberhard Karls University, Auf der Morgenstelle 32, D-72076 Tubingen, Germany.; Fujian Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agricultural and Forestry University, Fuzhou, Fujian 350002, China (L.Y.).; Division of Plant Science, School of Life Science, University of Dundee (at JHI), Invergowrie, Dundee DD2 5DA, United Kingdom Paul.Birch@hutton.ac.uk.
To be successful plant pathogens, microbes use "effector proteins" to manipulate host functions to their benefit. Identifying host targets of effector proteins and characterizing their role in the infection process allow us to better understand plant-pathogen interactions and the plant immune system. Yeast two-hybrid analysis and coimmunoprecipitation were used to demonstrate that the Phytophthora infestans effector AVIRULENCE 2 (PiAVR2) interacts with all three BRI1-SUPPRESSOR1-like (BSL) family members from potato (Solanum tuberosum). Transient expression of BSL1, BSL2, and BSL3 enhanced P. infestans leaf infection. BSL1 and BSL3 suppressed INFESTIN 1 elicitin-triggered cell death, showing that they negatively regulate immunity. Virus-induced gene silencing studies revealed that BSL2 and BSL3 are required for BSL1 stability and show that basal levels of immunity are increased in BSL-silenced plants. Immune suppression by BSL family members is dependent on the brassinosteroid-responsive host transcription factor CIB1/HBI1-like 1. The P. infestans effector PiAVR2 targets all three BSL family members in the crop plant S. tuberosum These phosphatases, known for their role in growth-promoting brassinosteroid signaling, all support P. infestans virulence and thus can be regarded as susceptibility factors in late blight infection.
PMID: 30782963
Plant Cell Environ , IF:6.362 , 2019 May , V42 (5) : P1615-1629 doi: 10.1111/pce.13510
DWARF4 accumulation in root tips is enhanced via blue light perception by cryptochromes.
Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, 153-8902, Japan.; Faculty of Agriculture, Kyushu University, Fukuoka, 819-0395, Japan.
Brassinosteroid (BR) signalling is known to be coordinated with light signalling in above ground tissue. Many studies focusing on the shade avoidance response in above ground tissue or hypocotyl elongation in darkness have revealed the contribution of the BR signalling pathway to these processes. We previously analysed the expression of DWARF 4 (DWF4), a key BR biosynthesis enzyme, and revealed that light perception in above ground tissues triggered DWF4 accumulation in root tips. To determine the required wavelength of light and photoreceptors responsible for this regulation, we studied DWF4-GUS marker plants grown in several monochromatic light conditions. We revealed that monochromatic blue LED light could induce DWF4 accumulation in primary root tips and root growth as much as white light, whereas monochromatic red LED could not. Consistent with this, a cryptochrome1/2 double mutant showed retarded root growth under white light whereas a phytochromeA/B double mutant did not. Taken together, our data strongly indicated that blue light signalling was important for DWF4 accumulation in root tips and root growth. Furthermore, DWF4 accumulation patterns in primary root tips were not altered by auxin or sugar treatment. Therefore, we hypothesize that blue light signalling from the shoot tissue is different from auxin and sugar signalling.
PMID: 30620085
J Integr Plant Biol , IF:4.885 , 2019 May , V61 (5) : P639-650 doi: 10.1111/jipb.12812
Transcriptome landscape of the early Brassica napus seed.
University of Manitoba, Winnipeg, Manitoba, Canada.
Brassica napus L. (canola) is one of the world's most economically important oilseeds. Despite our growing knowledge of Brassica genetics, we still know little about the genes and gene regulatory networks underlying early seed development. In this work, we use laser microdissection coupled with RNA sequencing to profile gene activity of both the maternal and filial subregions of the globular seed. We find subregions of the chalazal end including the chalazal endosperm, chalazal proliferating tissue, and chalazal seed coat, have unique transcriptome profiles associated with hormone biosynthesis and polysaccharide metabolism. We confirm that the chalazal seed coat is uniquely enriched for sucrose biosynthesis and transport, and that the chalazal endosperm may function as an important regulator of the maternal region through brassinosteroid synthesis. The chalazal proliferating tissue, a poorly understood subregion, was specifically enriched in transcripts associated with megasporogenesis and trehalose biosynthesis, suggesting this ephemeral structure plays an important role in both sporophytic development and carbon nutrient balance, respectively. Finally, compartmentalization of transcription factors and their regulatory circuits has uncovered previously unknown roles for the chalazal pole in early seed development.
PMID: 30941858
Int J Mol Sci , IF:4.556 , 2019 May , V20 (9) doi: 10.3390/ijms20092339
Involvement of BIG5 and BIG3 in BRI1 Trafficking Reveals Diverse Functions of BIG-subfamily ARF-GEFs in Plant Growth and Gravitropism.
Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. xueshan1984@yeah.net.; University of Chinese Academy of Sciences, Beijing 100049, China. xueshan1984@yeah.net.; Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. zoujunjie@caas.cn.; Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. liuyangfan@ibcas.ac.cn.; University of Chinese Academy of Sciences, Beijing 100049, China. liuyangfan@ibcas.ac.cn.; Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. ming.wang@genefirst.com.; University of Chinese Academy of Sciences, Beijing 100049, China. ming.wang@genefirst.com.; Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. chunxia.zhang@ibcas.ac.cn.; Key Laboratory of Plant Molecular Physiology, CAS Center for Excellence in Molecular Plant Sciences, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. lejie@ibcas.ac.cn.
ADP-ribosylation factor-guanine nucleotide exchange factors (ARF-GEFs) act as key regulators of vesicle trafficking in all eukaryotes. In Arabidopsis, there are eight ARF-GEFs, including three members of the GBF1 subfamily and five members of the BIG subfamily. These ARF-GEFs have different subcellular localizations and regulate different trafficking pathways. Until now, the roles of these BIG-subfamily ARF-GEFs have not been fully revealed. Here, analysis of the BIGs expression patterns showed that BIG3 and BIG5 have similar expression patterns. big5-1 displayed a dwarf growth and big3-1 big5-1 double mutant showed more severe defects, indicating functional redundancy between BIG3 and BIG5. Moreover, both big5-1 and big3-1 big5-1 exhibited a reduced sensitivity to Brassinosteroid (BR) treatment. Brefeldin A (BFA)-induced BR receptor Brassinosteroid insensitive 1 (BRI1) aggregation was reduced in big5-1 mutant, indicating that the action of BIG5 is required for BRI1 recycling. Furthermore, BR-induced dephosphorylation of transcription factor BZR1 was decreased in big3-1 big5-1 double mutants. The introduction of the gain-of-function of BZR1 mutant BZR1-1D in big3-1 big5-1 mutants can partially rescue the big3-1 big5-1 growth defects. Our findings revealed that BIG5 functions redundantly with BIG3 in plant growth and gravitropism, and BIG5 participates in BR signal transduction pathway through regulating BRI1 trafficking.
PMID: 31083521
Plant Cell Physiol , IF:4.062 , 2019 May , V60 (5) : P935-944 doi: 10.1093/pcp/pcz005
Brassinosteroid Induces Phosphorylation of the Plasma Membrane H+-ATPase during Hypocotyl Elongation in Arabidopsis thaliana.
Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa, Nagoya, Japan.; Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Chikusa, Nagoya, Japan.; Center for Gene Research, Nagoya University, Nagoya, Japan.
Brassinosteroids (BRs) are steroid phytohormones that regulate plant growth and development, and promote cell elongation at least in part via the acid-growth process. BRs have been suggested to induce cell elongation by the activating plasma membrane (PM) H+-ATPase. However, the mechanism by which BRs activate PM H+-ATPase has not been clarified. In this study, we investigated the effects of BR on hypocotyl elongation and the phosphorylation status of a penultimate residue, threonine, of PM H+-ATPase, which affects the activation, in the etiolated seedlings of Arabidopsis thaliana. Brassinolide (BL), an active endogenous BR, induced hypocotyl elongation, phosphorylation of the penultimate, threonine residue of PM H+-ATPase, and binding of the 14-3-3 protein to PM H+-ATPase in the endogenous BR-depleted seedlings. Changes in both BL-induced elongation and phosphorylation of PM H+-ATPase showed similar concentration dependency. BL did not induce phosphorylation of PM H+-ATPase in the BR receptor mutant bri1-6. In contrast, bikinin, a specific inhibitor of BIN2 that acts as a negative regulator of BR signaling, induced its phosphorylation. Furthermore, BL accumulated the transcripts of SMALL AUXIN UP RNA 9 (SAUR9) and SAUR19, which suppress dephosphorylation of the PM H+-ATPase penultimate residue by inhibiting D-clade type 2C protein phosphatase in the hypocotyls of etiolated seedlings. From these results, we conclude that BL-induced phosphorylation of PM H+-ATPase penultimate residue is mediated via the BRI1-BIN2 signaling pathway, together with the accumulation of SAURs during hypocotyl elongation.
PMID: 30649552
Rice (N Y) , IF:3.912 , 2019 May , V12 (1) : P35 doi: 10.1186/s12284-019-0287-9
Comparative study of the mycorrhizal root transcriptomes of wild and cultivated rice in response to the pathogen Magnaporthe oryzae.
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China.; University of Chinese Academy of Sciences, Beijing, 100049, China.; School of Life Sciences, Northeast Normal University, Changchun City, Jilin, China.; College of Life Science, Jilin Agricultural University, Changchun, Jilin, China.; Stress Adaptation Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22, Suehiro-cho, Tsurumi, Yokohama, 230-0045, Japan.; Stress Adaptation Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22, Suehiro-cho, Tsurumi, Yokohama, 230-0045, Japan. tranplamson@duytan.edu.vn.; Institute of Research and Development, Duy Tan University, 03 Quang Trung, Da Nang, 550000, Vietnam. tranplamson@duytan.edu.vn.; Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China. tiancj@neigae.ac.cn.
BACKGROUND: Rice, which serves as a staple food for more than half of the world's population, is very susceptible to the pathogenic fungus, Magnaporthe oryzae. However, common wild rice (Oryza rufipogon), which is the ancestor of Asian cultivated rice (O. sativa), has significant potential as a genetic source of resistance to M. oryzae. Recent studies have shown that the domestication of rice has altered its relationship to symbiotic arbuscular mycorrhizae. A comparative response of wild and domestic rice inhabited by mycorrhizae to infection by M. oryzae has not been documented. RESULTS: In the current study, roots of wild and cultivated rice colonized with the arbuscular mycorrhizal (AM) fungus (AMF) Rhizoglomus intraradices were used to compare the transcriptomic responses of the two species to infection by M. oryzae. Phenotypic analysis indicated that the colonization of wild and cultivated rice with R. intraradices improved the resistance of both genotypes to M. oryzae. Wild AM rice, however, was more resistant to M. oryzae than the cultivated AM rice, as well as nonmycorrhizal roots of wild rice. Transcriptome analysis indicated that the mechanisms regulating the responses of wild and cultivated AM rice to M. oryzae invasion were significantly different. The expression of a greater number of genes was changed in wild AM rice than in cultivated AM rice in response to the pathogen. Both wild and cultivated AM rice exhibited a shared response to M. oryzae which included genes related to the auxin and salicylic acid pathways; all of these play important roles in pathogenesis-related protein synthesis. In wild AM rice, secondary metabolic and biotic stress-related analyses indicated that the jasmonic acid synthesis-related alpha-linolenic acid pathway, the phenolic and terpenoid pathways, as well as the phenolic and terpenoid syntheses-related mevalonate (MVA) pathway were more affected by the pathogen. Genes related to these pathways were more significantly enriched in wild AM rice than in cultivated AM rice in response to M. oryzae. On the other hand, genes associated with the 'brassinosteroid biosynthesis' were more enriched in cultivated AM rice. CONCLUSIONS: The AMF R. intraradices-colonized rice plants exhibited greater resistance to M. oryzae than non-AMF-colonized plants. The findings of the current study demonstrate the potential effects of crop domestication on the benefits received by the host via root colonization with AMF(s), and provide new information on the underlying molecular mechanisms. In addition, results of this study can also help develop guidelines for the applications of AMF(s) when planting rice.
PMID: 31076886
Plant Physiol Biochem , IF:3.72 , 2019 May , V138 : P36-47 doi: 10.1016/j.plaphy.2019.02.014
Enhanced brassinosteroid signaling intensity via SlBRI1 overexpression negatively regulates drought resistance in a manner opposite of that via exogenous BR application in tomato.
State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China; Key Laboratory of Southwest China Wildlife Resources Conservation, China West Normal University, Nanchong, 637000, Sichuan, China.; State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China.; State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China. Electronic address: wangxff99@nwsuaf.edu.cn.
Brassinosteroids (BRs) regulate plant growth and stress responses. BRASSINOSTEROID-INSENSITIVE 1 (BRI1) is a BR receptor that perceives BRs and subsequently activates BR signaling. However, how BR contents and BRI1 expression levels affect the drought resistance of tomato requires further investigation. Here, we exogenously applied 24-epibrassinolide (EBR) and brassinazole (Brz) to tomato plants and generated different transgenic tomato SlBRI1 overexpression lines to study the drought stress response. Our results showed that EBR application 3 days before drought stress increased the contents of BRs and decreased abscisic acid (ABA) and reactive oxygen species (ROS), after which stomatal aperture and drought resistance eventually increased. Brz application reduced the drought resistance. Astonishingly, overexpression of 35S:SlBRI1, which increased BR signaling intensity, led to slightly improved contents of ABA and ROS and ultimately reduced both stomatal aperture and drought resistance. Moreover, plants expressing SlBRI1 driven by a stress-inducible promoter (Atrd29A) also exhibited reduced plant drought resistance. In all cases, enhancing the BR signaling intensity reduced antioxidant enzyme activity and reduced the expression of drought stress-related genes, ultimately compromising the drought resistance. Additionally, SlBRI1 mutants with altered brassinolide sensitivity (abs), which was weak BR signaling, exhibited significantly increased drought resistance. Therefore, our results reveal that BR contents positively regulated tomato drought resistance and that BR signaling intensity via BRI1 was negatively related to the drought resistance. These imply that the increased drought resistance in response to BRs is a newly discovered BR signaling branch that is located downstream of BRs and that differs from that of BRI1.
PMID: 30844693
BMC Plant Biol , IF:3.497 , 2019 May , V19 (1) : P220 doi: 10.1186/s12870-019-1832-9
BR deficiency causes increased sensitivity to drought and yield penalty in cotton.
State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China.; Zhengzhou Research base, State Key Laboratory of Cotton Biology, Zhengzhou University, Zhengzhou, 450000, China.; Zhengzhou Research base, State Key Laboratory of Cotton Biology, Zhengzhou University, Zhengzhou, 450000, China. aylifug@163.com.; State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China. aylifug@163.com.
BACKGROUND: Brassinosteroids (BRs) play crucial roles in drought tolerance, but the underlying molecular mechanisms remain unclear in the important oilseed and fiber crop, cotton (Gossypium hirsutum L.). RESULTS: To elucidate how BRs mediate drought tolerance in cotton, a cotton brassinosteroid (BR)-deficient mutant, pag1 (pagoda1), was employed for analysis. Importantly, the pag1 mutant showed increased sensitivity to drought stress, with shorter primary roots and fewer lateral roots. The number of stomata was significantly increased in the mutant, and the stomata aperture was much wider than that of the control plants. These mutant plants therefore showed an increased water loss rate. Furthermore, the abscisic acid (ABA) content, photosynthetic efficiency and starch content of the mutant were significantly lower than those of the wild type. The overall performance of the mutant plants was worse than that of the wild-type control under both normal and drought conditions. Moreover, Proteomic analysis revealed reduced levels of stress-related proteins in pag1 plants. CONCLUSIONS: These results suggest that BRs may modulate the drought tolerance of cotton by regulating much genes that related to drought stress and multiple organ responses to drought, including root growth, stomata development, the stomata aperture and photosynthesis. This study provides an important basis for understanding drought resistance regulated by BRs and cultivating drought-resistant cotton lines.
PMID: 31138186
BMC Plant Biol , IF:3.497 , 2019 May , V19 (1) : P191 doi: 10.1186/s12870-019-1783-1
Genome-wide identification, characterization, and expression patterns of the BZR transcription factor family in sugar beet (Beta vulgaris L.).
Sugar Beet Physiological Research Institute, Inner Mongolia Agricultural University, Hohhot, China.; Sugar Beet Physiological Research Institute, Inner Mongolia Agricultural University, Hohhot, China. syzh36@aliyun.com.
BACKGROUND: BRASSINAZOLE-RESISTANT (BZR) family genes encode plant-specific transcription factors (TFs) that participate in brassinosteroid signal transduction. BZR TFs have vital roles in plant growth, including cell elongation. However, little is known about BZR genes in sugar beet (Beta vulgaris L.). RESULTS: Therefore, we performed a genome-wide investigation of BvBZR genes in sugar beet. Through an analysis of the BES1_N conserved domain, six BvBZR gene family members were identified in the sugar beet genome, which clustered into three subgroups according to a phylogenetic analysis. Each clade was well defined by the conserved motifs, implying that close genetic relationships could be identified among the members of each subfamily. According to chromosomal distribution mapping, 2, 1, 1, 1, and 1 genes were located on chromosomes 1, 4, 5, 6, and 8, respectively. The cis-acting elements related to taproot growth were randomly distributed in the promoter sequences of the BvBZR genes. Tissue-specific expression analyses indicated that all BvBZR genes were expressed in all three major tissue types (roots, stems, and leaves), with significantly higher expression in leaves. Subcellular localization analysis revealed that Bv1_fxre and Bv6_nyuw are localized in the nuclei, consistent with the prediction of Wolf PSORT. CONCLUSION: These findings offer a basis to predict the functions of BZR genes in sugar beet, and lay a foundation for further research of the biological functions of BZR genes in sugar beet.
PMID: 31072335
Planta , IF:3.39 , 2019 May , V249 (5) : P1259-1266 doi: 10.1007/s00425-019-03112-7
Multifaceted plant G protein: interaction network, agronomic potential, and beyond.
Jiangsu Key Laboratory of Crop Genetics and Physiology/Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, Agricultural College of Yangzhou University, Yangzhou, 225009, China. wyj@yzu.edu.cn.; Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, 225009, China. wyj@yzu.edu.cn.; Jiangsu Key Laboratory of Crop Genetics and Physiology/Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, Agricultural College of Yangzhou University, Yangzhou, 225009, China.; Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, 225009, China.
MAIN CONCLUSION: Heterotrimeric G protein and interacting effectors are relevant for agronomic significance. We can manipulate G protein and effectors, individually or in combination, to develop plant ideotypes by intelligent design breeding. Heterotrimeric guanine nucleotide-binding protein (G protein) is involved in a wide range of biological events, many of which with agronomic significance. In this review, we summarize recent advances of plant G protein research. We first retrieve maize G protein core subunits Galpha, Gbeta, and Ggamma based on information of Arabidopsis and rice G proteins using integrated BLAST and domain confirmation. Then, we briefly introduce the distribution and function of G protein. We also describe the interaction between G protein and CLAVATA receptor, brassinosteroid signaling kinase complex, and MADS-domain transcription factor. Finally, we discuss the application of G protein knowledge in intelligent plant breeding with focus on the improvement of agronomically important traits.
PMID: 30790051
Planta , IF:3.39 , 2019 May , V249 (5) : P1391-1403 doi: 10.1007/s00425-019-03094-6
Brassinosteroids facilitate xylem differentiation and wood formation in tomato.
Department of Biology, Chungbuk National University, Cheongju, 28644, Republic of Korea.; National Agrobiodiversity Center, National Academy of Agricultural Science RDA, Jeonju, 54875, Republic of Korea.; Department of Information and Statistics, Chungbuk National University, Cheongju, 28644, Republic of Korea.; Department of Industrial Plant Science and Technology, Chungbuk National University, Cheongju, 28644, Republic of Korea.; Department of Horticultural Bioscience, College of Natural Resource and Life Science, Pusan National University, Miryang, 50467, Republic of Korea.; Department of Biotechnology, Duksung Women's University, Seoul, 01369, Republic of Korea.; Department of Forest Bio-Resources, National Institute of Forest Science, Suwon, 16631, Republic of Korea.; Division of Biological Sciences, Research Institute for Basic Science, Wonkwang University, Iksan, 54538, Republic of Korea.; Department of Biology, Chungbuk National University, Cheongju, 28644, Republic of Korea. hjryu96@gmail.com.
MAIN CONCLUSION: BR signaling pathways facilitate xylem differentiation and wood formation by fine tuning SlBZR1/SlBZR2-mediated gene expression networks involved in plant secondary growth. Brassinosteroid (BR) signaling and BR crosstalk with diverse signaling cues are involved in the pleiotropic regulation of plant growth and development. Recent studies reported the critical roles of BR biosynthesis and signaling in vascular bundle development and plant secondary growth; however, the molecular bases of these roles are unclear. Here, we performed comparative physiological and anatomical analyses of shoot morphological growth in a cultivated wild-type tomato (Solanum lycopersicum cv. BGA) and a BR biosynthetic mutant [Micro Tom (MT)]. We observed that the canonical BR signaling pathway was essential for xylem differentiation and sequential wood formation by facilitating plant secondary growth. The gradual retardation of xylem development phenotypes during shoot vegetative growth in the BR-deficient MT tomato mutant recovered completely in response to exogenous BR treatment or genetic complementation of the BR biosynthetic DWARF (D) gene. By contrast, overexpression of the tomato Glycogen synthase kinase 3 (SlGSK3) or CRISPR-Cas9 (CR)-mediated knockout of the tomato Brassinosteroid-insensitive 1 (SlBRI1) impaired BR signaling and resulted in severely defective xylem differentiation and secondary growth. Genetic modulation of the transcriptional activity of the tomato Brassinazole-resistant 1/2 (SlBZR1/SlBZR2) confirmed the positive roles of BR signaling pathways for xylem differentiation and secondary growth. Our data indicate that BR signaling pathways directly promote xylem differentiation and wood formation by canonical BR-activated SlBZR1/SlBZR2.
PMID: 30673841