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Introduction
We study the regulatory circuits in plants using mostly proteomic and genomic approaches. We focus on brassinosteroid hormone, receptor kinases, transcription networks, and plant development
Current institution
Additional affiliations
February 2018 - January 2019
July 2001 - present
July 2001 - present
Education
August 1992 - January 1998
Publications
Publications (202)
Plants are equipped with the capacity to respond to a large number of diverse signals, both internal ones and those emanating from the environment, that are critical to their survival and adaption as sessile organisms. These signals need to be integrated through highly structured intracellular networks to ensure coherent cellular responses, and in...
For maintenance of cellular homeostasis, the actions of growth-promoting hormones must be attenuated when nutrient and energy become limiting. The molecular mechanisms that coordinate hormone-dependent growth responses with nutrient availability remain poorly understood in plants [1, 2]. The target of rapamycin (TOR) kinase is an evolutionarily con...
The spatiotemporal balance between stem cell maintenance, proliferation, and differentiation determines the rate of root growth and is controlled by hormones, including auxin and brassinosteroid (BR). However, the spatial actions of BR and its interactions with auxin remain unclear in roots. Here, we show that oppositely patterned and antagonistic...
Brassinosteroid and gibberellin promote many similar developmental responses in plants; however, their relationship remains unclear. Here we show that BR and GA act interdependently through a direct interaction between the BR-activated BZR1 and GA-inactivated DELLA transcription regulators. GA promotion of cell elongation required BR signalling, wh...
Post-translational modi cations of nucleocytoplasmic proteins by O-linked beta-N-acetylglucosamine (O-GlcNAc) and O-linked fucose (O-fucose) are emerging as key signaling mechanisms in plants. O-fucosylation and O-GlcNAcylation are catalyzed by SPINDLY (SPY) and SECRET AGENT (SEC), respectively, which are redundantly essential for viability and gro...
Alternative splicing (AS) is a key mechanism of gene regulation, but the full repertoire of proteins involved and the regulatory mechanisms governing this process remain poorly understood. Using TurboID-based proximity labeling coupled with mass spectrometry (PL-MS), we comprehensively mapped the Arabidopsis AS machinery, focusing on the evolutiona...
Nuclear protein delivery underlies an array of biotechnological and therapeutic applications. While many variations of protein delivery methods have been described, it can still be difficult or inefficient to introduce exogenous proteins into plants. A major barrier to progress is the cell wall which is primarily composed of polysaccharides and thu...
Ethylene plays its essential roles in plant development, growth, and defense responses by controlling the transcriptional reprograming, in which EIN2-C–directed regulation of histone acetylation is the first key step for chromatin to perceive ethylene signaling. But how the nuclear acetyl coenzyme A (acetyl CoA) is produced to ensure the ethylene-m...
Plants often adapt to adverse or stress conditions via differential growth. The trans-Golgi network (TGN) has been implicated in stress responses, but it is not clear in what capacity it mediates adaptive growth decisions. In this study, we assess the role of the TGN in stress responses by exploring the previously identified interactome of the Tran...
Protein O-glycosylation is a nutrient signaling mechanism that plays an essential role in maintaining cellular homeostasis across different species. In plants, SPINDLY (SPY) and SECRET AGENT (SEC) posttranslationally modify hundreds of intracellular proteins with O-fucose and O-linked N-acetylglucosamine, respectively. SPY and SEC play overlapping...
Ethylene plays its essential roles in plant development, growth, and defense responses by controlling the transcriptional reprograming, in which EIN2-C-directed regulation of histone acetylation is the first key-step for chromatin to perceive ethylene signaling. But how the nuclear acetyl coenzyme A (acetyl CoA) is produced to ensure the ethylene-m...
BRASSINAZONE RESISTANT 1 (BZR1) is a key transcription factor of the brassinosteroid signaling pathway but also a signaling hub that integrates diverse signals that modulate plant growth. Previous studies have shown that starvation causes BZR1 degradation, but the underlying mechanisms are not understood. Here we performed quantitative proteomic an...
Plant cell expansion is driven by turgor pressure and regulated by hormones. How plant cells avoid cell wall rupture during hormone-induced cell expansion remains a mystery. Here we show that brassinosteroid (BR), while stimulating cell elongation, promotes the plasma membrane (PM) accumulation of the receptor kinase FERONIA (FER), which monitors c...
The brassinosteroid (BR) hormone is a central modulator of plant growth, development, and responses to stresses by activating or repressing the expression of thousands of genes through the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1) and its homologues. However, the molecular mechanism that determines the transcriptional activation versus r...
Background
Genetic variation in regulatory sequences that alter transcription factor (TF) binding is a major cause of phenotypic diversity. Brassinosteroid is a growth hormone that has major effects on plant phenotypes. Genetic variation in brassinosteroid-responsive cis-elements likely contributes to trait variation. Pinpointing such regulatory va...
The recent discovery of SPINDLY (SPY)-catalyzed protein O-fucosylation revealed a novel mechanism for regulating nucleocytoplasmic protein functions in plants. Genetic evidence indicates important roles of SPY in diverse developmental and physiological processes. However, the upstream signal controlling SPY activity and the downstream substrate pro...
Elucidating enzyme-substrate relationships in posttranslational modification (PTM) networks is crucial for understanding signal transduction pathways but is technically difficult because enzyme-substrate interactions tend to be transient. Here we demonstrate that TurboID-based proximity labeling (TbPL) effectively and specifically captures the subs...
Background:
There are several mechanisms believed to be essential for the development of distant metastasis in lung adenocarcinoma (LUAD), but the prediction of distant metastasis is still a challenge. The purpose of the present study was to examine the specific changes in RNA expression, including long non-coding RNAs (lncRNAs) in distant metasta...
Hundreds of leucine-rich repeat receptor kinases (LRR-RKs) have evolved to control diverse processes of growth, development and immunity in plants, but the mechanisms that link LRR-RKs to distinct cellular responses are not understood. Here we show that two LRR-RKs, the brassinosteroid hormone receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) and the f...
Rates of plant cell elongation change with day-night alternation, reflecting differences in metabolism related to cell wall remodeling. Information from cell wall surveillance pathways must be integrated with growth regulation pathways to provide feedback regulation of cell wall modification; such feedback regulation is important to ensure sufficie...
Metabolic labeling using stable isotopes is widely used for the relative quantification of proteins in proteomic studies. In plants, metabolic labeling using ¹⁵N has great potential, but the associated complexity of data analysis has limited its usage. Here, we present the ¹⁵N stable-isotope labeled protein quantification workflow utilizing open-ac...
Metabolic labeling using stable isotopes is widely used for the relative quantification of proteins in proteomic studies. In plants, metabolic labeling using 15N has great potential, but the associated complexity of data analysis has limited its usage. Here, we present the 15N stable-isotope labeled protein quantification workflow utilizing open-ac...
Variation in transcriptional regulation is a major cause of phenotypic diversity. Genome-wide association studies (GWAS) have shown that most functional variants reside in non-coding regions, where they potentially affect transcription factor (TF) binding and chromatin accessibility to alter gene expression. Pinpointing such regulatory variations,...
Sugar, light, and hormones are major signals regulating plant growth and development, however, the interactions among these signals are not fully understood at the molecular level. Recent studies showed that sugar promotes hypocotyl elongation by activating the brassinosteroid (BR) signaling pathway after shifting Arabidopsis seedlings from light t...
Asymmetric cell division (ACD) requires protein polarization in the mother cell to produce daughter cells with distinct identities (cell-fate asymmetry). Here, we define a previously undocumented mechanism for establishing cell-fate asymmetry in Arabidopsis stomatal stem cells. In particular, we show that polarization of the protein phosphatase BSL...
Growth control in eukaryotes depends on the TOR kinase, which integrates energy and nutrient signals. In this issue of Developmental Cell, Liu et al. demonstrate that, in plants, inorganic nitrogen and amino acids activate TOR via the GTPase ROP2 to promote cell proliferation and leaf growth in the shoot.
In flowering plants, repression of the seed maturation program is essential for the transition from the seed to the vegetative phase, but the underlying mechanisms remain poorly understood. The B3-domain protein VIVIPAROUS1/ABSCISIC ACID INSENSITIVE3-LIKE 1 (VAL1) is involved in repressing the seed maturation program. Here we uncovered a molecular...
O-GlcNAc modification plays important roles in metabolic regulation of cellular status. Two homologs of O-GlcNAc transferase, SECRET AGENT (SEC) and SPINDLY (SPY), which have O-GlcNAc and O-fucosyl transferase activities, respectively, are essential in Arabidopsis but have largely unknown cellular targets. Here we show that AtACINUS is O-GlcNAcylat...
Soybean (Glycine max L.) is a major crop providing important source for protein and oil for human life. Low phosphate (LP) availability is a critical limiting factor affecting soybean production. Soybean plants develop a series of strategies to adapt to phosphate (Pi) limitation condition. However, the underlying molecular mechanisms responsible fo...
O-GlcNAc modification plays important roles in metabolic regulation of cellular status. Two homologs of O-GlcNAc transferase, SECRET AGENT (SEC) and SPINDLY (SPY), which have O-GlcNAc and O-fucosyl transferase activities, respectively, are essential in Arabidopsis but have largely unknown cellular targets. Here we show that AtACINUS is O-GlcNAcylat...
Asymmetric cell division (ACD) often requires protein polarization in the mother cell to produce daughter cells with distinct identities (“cell-fate asymmetry”). Here, we define a previously undocumented mechanism for establishing cell-fate asymmetry in Arabidopsis stomatal stem cells. In particular, we show that polarization of BSL protein phospha...
Main conclusion:
This study demonstrates that brassinosteroid is essential for seedling and shoot growth in moso bamboo. The shoot of moso bamboo is known to grow extremely fast. The roles of phytohormones in such fast growth of bamboo shoot remain unclear. Here we reported that endogenous brassinosteroid (BR) is a major factor promoting bamboo sh...
How the membrane trafficking system spatially organizes intracellular activities and intercellular signaling networks is not well understood in plants. The TRAnsport Protein Particle (TRAPP) complexes play key roles in selective delivery of membrane vesicles to various subcellular compartments in yeast and animals, but are not characterized in plan...
Key message
PSBR1 is a moso bamboo gene negatively regulated by brassinosteroid, which encodes a mitochondrial localized protein. Overexpression of PSBR1 leads to growth inhibition in various growth progresses in Arabidopsis.
Abstract
The young shoot of moso bamboo (Phyllostachys edulis) is known as one of the fastest growing plant organs. The rol...
As a group of plant-specific proteins, OVATE family protein (OFP) members have been shown to function as transcriptional repressors and involve in plant growth regulation in Arabidopsis and rice. It has also been shown that OFPs can interact with TONNEAU1 Recruiting Motif (TRM) proteins to regulate tomato fruit shape. In this study, we show that mu...
Auxin and brassinosteroids (BR) are crucial growth regulators and display overlapping functions during plant development. Here, we reveal an alternative phytohormone crosstalk mechanism, revealing that BR signaling controls PIN-LIKES (PILS)-dependent nuclear abundance of auxin. We performed a forward genetic screen for imperial pils (imp) mutants t...
The American biologist Winslow Russel Briggs (1928–2019) was a global leader in plant physiology, genetics and photobiology. In this contribution, we try to share our knowledge of the remarkable career of this outstanding scientist. After earning his PhD at Harvard (Cambridge, Massachusetts), he started his independent research program at Stanford...
Abstract
The American biologist Winslow Russel Briggs (1928–2019) was a global leader in plant physiology, genetics and photobiology. In this contribution, we try to share our knowledge of the remarkable career of this outstanding scientist. After earning his PhD at Harvard (Cambridge, Massachusetts), he started his independent research program at...
How the membrane trafficking system spatially organizes intracellular activities and intercellular signaling networks is not well understood in plants. The Transport Protein Particle (TRAPP) complexes play key roles in selective delivery of membrane vesicles to various subcellular compartments in yeast and animals, but remain to be fully characteri...
Among the hundreds of receptor-like kinases (RLKs) in plants, the brassinosteroid (BR) hormone receptor BR-INSENSITIVE 1 (BRI1) and the immunity receptor FLAGELLIN SENSING 2 (FLS2) share a common co-receptor kinase, but lead to distinct growth and immunity responses, respectively. Here we show that the BSU1 family of phosphatases, known to mediate...
The receptor-like kinase SIT1 acts as a sensor in rice (Oryza sativa) roots, relaying salt stress signals via elevated kinase activity to enhance salt sensitivity. Here, we demonstrate that Protein Phosphatase 2A (PP2A) regulatory subunit B'κ constrains SIT1 activity under salt stress. B'κ-PP2A deactivates SIT1 directly by dephosphorylating the kin...
Transient protein-protein interactions (PPIs), such as those between posttranslational modifying enzymes and their substrates, play key roles in cellular regulation, but are difficult to identify. Here we demonstrate the application of enzyme-catalyzed proximity labeling (PL), using the engineered promiscuous biotin ligase TurboID, as a sensitive m...
Background
Brassinosteroids (BRs) play a crucial role in plant vegetative growth and reproductive development. The transcription factors BZR1 and BES1/BZR2 are well characterized as downstream regulators of the BR signaling pathway in Arabidopsis and rice. Soybean contains four BZR1-like proteins (GmBZLs), and it was reported that GmBZL2 plays a co...
Evidence suggests that Helicobacter pylori (H. pylori) is not only the main cause of gastric cancer (GC), but is also closely associated with its metastasis. One of the major virulence factors in H. pylori is the cytotoxin-associated gene A (CagA). With the growing proportion of amoxicillin-resistant H. pylori strains, the present study aimed to ex...
Hydrogen peroxide (H2O2) is an important signaling molecule in plant developmental processes and stress responses. However, whether H2O2-mediated signaling crosstalks with plant hormone signaling is largely unclear. Here, we show that H2O2induces the oxidation of the BRASSINAZOLE-RESISTANT1 (BZR1) transcription factor, which functions as a master r...
The work conducted by the US Department of Energy (DOE) Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the US DOE under Contract DE-AC02-05CH11231 (to S.H.B., E.G., A.R.G., and J.W.S.). Other major research support was provided by NSF 0929558 (to S.H.B. and A.R.G.); National Oceanic and Atmo...
The glycogen synthase kinase-3 (GSK3) family kinases are central cellular regulators highly conserved in all eukaryotes. In Arabidopsis, the GSK3-like kinase BIN2 phosphorylates a range of proteins to control broad developmental processes, and BIN2 is degraded through unknown mechanism upon receptor kinase-mediated brassinosteroid (BR) signaling. H...
Upon light-induced nuclear translocation, phytochrome (phy) sensory photoreceptors interact with, and induce rapid phosphorylation and consequent ubiquitin-mediated degradation of, transcription factors, called PIFs, thereby regulating target gene expression and plant development. Nevertheless, the biochemical mechanism of phy-induced PIF phosphory...
Supplementary Figures and Supplementary Table
In 2009, the draft genome of the reference inbred line of maize (Zea mays L. spp. mays cv. B73) was published so that, using this specific corn variety, molecular analyses of physiological processes became possible. However, the morphology and developmental patterns of B73 maize, compared with that of the more frequently used hybrid varieties, have...
Significance
Studies in mammalian systems have shown important functions of O-linked N -acetylglucosamine (O-GlcNAc) modification of proteins (O-GlcNAcylation) in a wide range of cellular, physiological, and disease processes. Genetic evidence indicates that O-GlcNAcylation is essential for plant growth and development. However, very few O-GlcNAc–m...
Arabidopsis adapts to elevated temperature by promoting stem elongation and hyponastic growth through a temperature-responsive transcription factor PIF4. Here we show that the evening-expressed clock component TOC1 interacts with and inactivates PIF4, thereby suppressing thermoresponsive growth in the evening. We find that the expression of PIF4 ta...
Supplementary Figures 1 - 10 and Supplementary Table 1
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Plant growth is controlled by integration of hormonal and light-signaling pathways. BZS1 is a B-box zinc finger protein previously characterized as a negative regulator in the brassinosteroid (BR) signaling pathway and positive regulator in the light-signaling pathway. However, the mechanisms by which BZS1/BBX20 integrates light and hormonal pathwa...
SWI/SNF-type chromatin remodelers, such as BRAHMA (BRM), and H3K27 demethylases both have active roles in regulating gene expression at the chromatin level, but how they are recruited to specific genomic sites remains largely unknown. Here we show that RELATIVE OF EARLY FLOWERING 6 (REF6), a plant-unique H3K27 demethylase, targets genomic loci cont...
This study presents the first large scale analysis of plant intact glycopeptides. Using wheat germ agglutinin lectin weak affinity chromatography to enrich modified peptides, followed by ETD fragmentation tandem mass spectrometry, glycan compositions on over 1100 glycopeptides from 270 proteins found in Arabidopsis inflorescence tissue were charact...
Mutation of the immunophilin-like FK506-binding protein TWISTED DWARF1 (FKBP42/TWD1) causes dwarf and twisted-organ phenotypes in Arabidopsis. However, the function of FKBP42 is not fully understood at the molecular level. Using genetic, physiological and immunological experiments, we show here that FKBP42 is necessary for brassinosteroid (BR) sign...
Brassinosteroid (BR) binding activates the receptor kinase BRI1 by inducing heterodimerization with its co-receptor kinase BAK1; however, the mechanisms that reversibly inactivate BRI1 remain unclear. Here we show that cytoplasm-localized PP2A B' regulatory subunits interact with BRI1 to mediate its dephosphorylation and inactivation. Loss-of-funct...
Rice is the most tolerant staple crop to aluminum (Al) toxicity, which is a limiting stress for grain production worldwide. This Al tolerance is the result of combined mechanisms that are triggered in part by the transcription factor ASR5. ASRs are dual target proteins that participate as chaperones in the cytoplasm and as transcription factors in...
Steroid hormones are key regulators of growth and physiology in both plants and animals. The plant steroid hormones known as brassinosteroids (BRs) are essential for a wide range of developmental processes throughout the life cycle. In contrast with animal steroid hormones, which act mostly through nuclear receptors, BRs act through a cell-surface...
Brassinosteroid (BR) regulates diverse physiological and developmental processes in plants (Choudhary et al., 2012). BR binds to the receptor kinase BRI1 to trigger a phosphorylation/dephosphorylation cascade, which includes phosphorylation of Brassinosteroid Signaling Kinase 1 (BSK1) and Constitutive Differential Growth 1 (CDG1) by BRI1, phosphory...
Vascular tissues are very important for providing both mechanical strength and long-distance transport. The molecular mechanisms of regulation of vascular tissue development are still not fully understood. In this study we identified ANAC005 as a membrane-associated NAC family transcription factor that regulates vascular tissue development. Reporte...
The shoot of grass coleoptiles consists of the mesocotyl, the node, and the coleoptile (with enclosed primary leaf). Since the 1930s, it is known that auxin (indole-3-acetic acid, IAA), produced in the tip of the coleoptile, is the central regulator of turgor-driven organ growth. Fifty years ago, it was discovered that antibiotics that suppress pro...
One of the major constraints on crop production is the ability of plants to grow in acidic soils, where aluminum (Al) is soluble in its toxic form (Al3+). However, some plants can address this Al toxicity by utilizing different strategies such as exclusion (an external mechanism) and detoxification (an internal mechanism). Rice, an important food s...
Brassinosteroid (BR) regulates plant development by activating the transcription factor brassinazole resistant 1 (BZR1), which activates and represses different target genes to switch cellular programmes. The mechanisms that determine BZR1's transcriptional activities remain largely unknown. Here we show that BZR1 represses target genes by recruiti...
After light-induced nuclear translocation, phytochrome photoreceptors interact with and induce rapid phosphorylation and degradation
of basic helix-loop-helix transcription factors, such as PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), to regulate gene expression.
Concomitantly, this interaction triggers feedback reduction of phytochrome B (phyB) levels...
BR-regulated genes in wild type and their BR-responsive expression in the iaa3 mutant.Seedlings were grown on 2 µM propiconazole medium for 5 days in the dark and treated with mock or 100 nM brassinolide (BL) for 4 hr. BR-regulated genes were defined by 1.5-fold difference between wild type (+BL) and wild type (−BL) with p-value<0.01.DOI:
http://dx...
Primer list for qRT-PCR, ChIP-PCR and DNA pull-down assays.
DOI:
http://dx.doi.org/10.7554/eLife.03031.023
(A) ARF6 target genes. ChIP-Seq analysis R (CSAR) software was used to identify binding peaks, with parameters (backg = 10, norm = −1, test = 'Ratio', times = 1e6, digits = 2) (Muino et al., 2011). Binding peaks with FDR <0.01 were finally defined as the ARF6 binding peak and genes having at least one ARF6 binding peak within its promoter (−3 kb) o...
Auxin-activated genes previously identified in hypocotyls (Chapman et al., 2012) were compared with ARF6 target genes identified by ChIP-Seq to identify the auxin-activated ARF6 target genes in hypocotyls.30 or 120 min: genes are activated after 30 or 120 min of auxin treatment.DOI:
http://dx.doi.org/10.7554/eLife.03031.005
Genes whose expression levels are affected in the iaa3 mutant.Seedlings of wild type and iaa3 were grown on 2 µM propiconazole medium for 5 days in the dark and treated with 100 nM brassinolide for 4 hr. The IAA3-regulated genes were defined by 1.5-fold difference between iaa3 and wild type with p<0.01.DOI:
http://dx.doi.org/10.7554/eLife.03031.013
Plants adapt to environmental light conditions by photoreceptor-mediated physiological responses, but the mechanism by which photoreceptors perceive and transduce the signals is still unresolved. Here, we used 2-D difference gel electrophoresis (2-D DIGE) and mass spectrometry to characterize early molecular events induced by short blue-light expos...
The tradeoff between growth and immunity is regulated by integrating hormonal cues, biotic signals, and developmental programs, and is fine-tuned to maximize organismal growth and survival. Four recent papers, including Chandran et al. (2014) in this issue of Cell Host & Microbe, provide insights into the underlying mechanisms in plants.
Unlike many wild grasses, domesticated rice cultivars have uniform culm height and panicle size among tillers and the main shoot, which is an important trait for grain yield. However, the genetic basis of this trait remains unknown. Here, we report that DWARF TILLER1 (DWT1) controls the developmental uniformity of the main shoot and tillers in rice...
The trade-off between growth and immunity is crucial for survival in plants. However, the mechanism underlying growth-immunity balance has remained elusive. The PRE-IBH1-HBI1 tripartite helix-loop-helix/basic helix-loop-helix module is part of a central transcription network that mediates growth regulation by several hormonal and environmental sign...
