Giltsu Choi

Chungnam National University, Daiden, Daejeon, South Korea

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Publications (45)327.88 Total impact

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    ABSTRACT: Ginseng is a medicinal herb that requires cultivation under shade conditions, typically for 4-6 yr, before harvesting. The principal components of ginseng are ginsenosides, glycosylated tetracyclic terpenes. Dammarene-type ginsenosides are classified into two groups, protopanaxadiol (PPD) and protopanaxatriol (PPT), based on their hydroxylation patterns, and further diverge to diverse ginsenosides through differential glycosylation. Three early enzymes, Dammarenediol-II synthase (DS) and two P450 enzymes, protopanaxadiol synthase (PPDS) and protopanaxatriol synthase (PPTS), have been reported, but glycosyltransferases that are necessary to synthesize specific ginsenosides have not yet been fully identified. To discover glycosyltransferases responsible for ginsenoside biosynthesis, we sequenced and assembled the ginseng transcriptome de novo and characterized two UDP-glycosyltransferases (PgUGTs): PgUGT74AE2 and PgUGT94Q2. PgUGT74AE2 transfers a glucose moiety from UDP-glucose (UDP-Glc) to the C3 hydroxyl groups of PPD and compound K to form Rh2 and F2, respectively, whereas PgUGT94Q2 transfers a glucose moiety from UDP-Glc to Rh2 and F2 to form Rg3 and Rd, respectively. Introduction of the two UGTs into yeast together with PgDS and PgPPDS resulted in the de novo production of Rg3. Our results indicate that these two UGTs are key enzymes for the synthesis of ginsenosides and provide a method for producing specific ginsenosides through yeast fermentation.
    Plant and Cell Physiology 10/2014; · 4.98 Impact Factor
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    ABSTRACT: Phytochrome-Interacting Factor 1 (PIF1) inhibits light-dependent seed germination. The specific function of PIF1 in seed germination is partly due to its high-level expression in imbibed seeds, but the associated regulatory factors have not been identified. Here, we show that mutation of the EFS gene, encoding an H3K4 and H3K36 methyltransferase, decreases the level of H3K36me2 and H3K36me3 but not H3K4me3 at the PIF1 locus, reduces the targeting of RNA polymerase II to the PIF1 locus, and reduces the mRNA expression of PIF1 in imbibed seeds. Consistently, the efs mutant geminated even under the phyBoff condition, and had the expression profiles of PIF1 target genes similar to that of the pif1 mutant. Introduction of an EFS transgene into the efs mutant restored the level of H3K36me2 and H3K36me3 at the PIF1 locus, the high-level expression of PIF1 mRNA, the expression pattern of PIF1 target genes, and the light-dependent germination of these seeds. Introduction of a PIF1 transgene into the efs mutant also restored the expression pattern of PIF1 target genes and light-dependent germination in imbibed seeds, but not flowering phenotype. Taken together, our results indicate that EFS is necessary for high-level expression of the PIF1 mRNA in imbibed seeds.
    The Plant Journal 02/2014; · 6.58 Impact Factor
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    ABSTRACT: Plants initiate senescence to shed photosynthetically inefficient leaves. Light deprivation induces leaf senescence, which involves massive transcriptional reprogramming to dismantle cellular components and remobilize nutrients. In darkness, intermittent pulses of red light can inhibit senescence, likely via phytochromes. However, the precise molecular mechanisms transducing the signals from light perception to the inhibition of senescence remain elusive. Here, we show that in Arabidopsis, dark-induced senescence requires phytochrome-interacting transcription factors PIF4 and PIF5 (PIF4/PIF5). ELF3 and phytochrome B inhibit senescence by repressing PIF4/PIF5 at the transcriptional and post-translational levels, respectively. PIF4/PIF5 act in the signalling pathways of two senescence-promoting hormones, ethylene and abscisic acid, by directly activating expression of EIN3, ABI5 and EEL. In turn, PIF4, PIF5, EIN3, ABI5 and EEL directly activate the expression of the major senescence-promoting NAC transcription factor ORESARA1, thus forming multiple, coherent feed-forward loops. Our results reveal how classical light signalling connects to senescence in Arabidopsis.
    Nature Communications 01/2014; 5:4636. · 10.74 Impact Factor
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    ABSTRACT: Seeds monitor the environment to germinate at the proper time, but different species respond differently to environmental conditions, particularly light and temperature. In Arabidopsis thaliana, light promotes germination but high temperature suppresses germination. We previously reported that light promotes germination by repressing SOMNUS (SOM). Here, we examined whether high temperature also regulates germination through SOM and found that high temperature activates SOM expression. Consistent with this, som mutants germinated more frequently than the wild type at high temperature. The induction of SOM mRNA at high temperature required abscisic acid (ABA) and gibberellic acid biosynthesis, and ABA-INSENSITIVE3 (ABI3), ABI5, and DELLAs positively regulated SOM expression. Chromatin immunoprecipitation assays indicated that ABI3, ABI5, and DELLAs all target the SOM promoter. At the protein level, ABI3, ABI5, and DELLAs all interact with each other, suggesting that they form a complex on the SOM promoter to activate SOM expression at high temperature. We found that high-temperature-inducible genes frequently have RY motifs and ABA-responsive elements in their promoters, some of which are targeted by ABI3, ABI5, and DELLAs in vivo. Taken together, our data indicate that ABI3, ABI5, and DELLAs mediate high-temperature signaling to activate the expression of SOM and other high-temperature-inducible genes, thereby inhibiting seed germination.
    The Plant Cell 12/2013; · 9.25 Impact Factor
  • Jinkil Jeong, Giltsu Choi
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    ABSTRACT: Phytochromes are plant photoreceptors that perceive red and far-red light. Upon the perception of light in Arabidopsis, light-activated phytochromes enter the nucleus and act on a set of interacting proteins, modulating their activities and thereby altering the expression levels of ∼10% of the organism's entire gene complement. Phytochromeinteracting factors (PIFs) belonging to Arabidopsis basic helix-loop-helix (bHLH) subgroup 15 are key interacting proteins that play negative roles in light responses. Their activities are post-translationally countered by light-activated phytochromes, which promote the degradation of PIFs and directly or indirectly inhibit their binding to DNA. The PIFs share a high degree of similarity, but examinations of pif single and multiple mutants have indicated that they have shared and distinct functions in various developmental and physiological processes. These are believed to stem from differences in both intrinsic protein properties and their gene expression patterns. In an effort to clarify the basis of these shared and distinct functions, we compared recently published genome-wide ChIP data, developmental gene expression maps, and responses to various stimuli for the various PIFs. Based on our observations, we propose that the biological roles of PIFs stem from their shared and distinct DNA binding targets and specific gene expression patterns.
    Molecules and Cells 05/2013; 35(5):371-380. · 2.21 Impact Factor
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    ABSTRACT: Several positive transcription factors regulate Arabidopsis anthocyanin biosynthesis. HY5, a component of light-signaling pathways, and PAP1, an R2R3-MYB transcription factor, share common regulatory targets on anthocyanin biosynthesis genes. The epistatic interactions between the two transcription factors are currently unknown. To address this problem, we analyzed crosses between hy5 and pap1 mutants (hy5pap1) or pap1D overexpressors (hy5pap1D), performed chromatin immunoprecipitation-qPCR, and determined the PAP1 promoter region through deletion analysis. The results show that HY5 regulates PAP1 expression via direct binding to G- and ACE-boxes in the promoter region, which suggests bifurcate regulation of anthocyanin biosynthesis by HY5 via transcriptional activation of PAP1.
    FEBS letters 04/2013; · 3.54 Impact Factor
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    ABSTRACT: DELLA proteins, consisting of GA INSENSITIVE, REPRESSOR OF GA1-3, RGA-LIKE1 (RGL1), RGL2, and RGL3, are central repressors of gibberellin (GA) responses, but their molecular functions are not fully understood. We isolated four DELLA-interacting RING domain proteins, previously designated as BOTRYTIS SUSCEPTIBLE1 INTERACTOR (BOI), BOI-RELATED GENE1 (BRG1), BRG2, and BRG3 (collectively referred to as BOIs). Single mutants of each BOI gene failed to significantly alter GA responses, but the boi quadruple mutant (boiQ) showed a higher seed germination frequency in the presence of paclobutrazol, precocious juvenile-to-adult phase transition, and early flowering, all of which are consistent with enhanced GA signaling. By contrast, BOI overexpression lines displayed phenotypes consistent with reduced GA signaling. Analysis of a gai-1 boiQ pentuple mutant further indicated that the GAI protein requires BOIs to inhibit a subset of GA responses. At the molecular level, BOIs did not significantly alter the stability of a DELLA protein. Instead, BOI and DELLA proteins are targeted to the promoters of a subset of GA-responsive genes and repress their expression. Taken together, our results indicate that the DELLA and BOI proteins inhibit GA responses by interacting with each other, binding to the same promoters of GA-responsive genes, and repressing these genes.
    The Plant Cell 03/2013; · 9.25 Impact Factor
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    ABSTRACT: Seed dormancy, a seed status that prohibits germination even in the presence of inductive germination signals, is a poorly understood process. To identify molecular components that regulate seed dormancy, we screened T-DNA insertion lines and identified a mutant designated honsu (hon). HON loss-of-function mutants display deep seed dormancy, whereas HON-overexpressing lines display shallow seed dormancy. HON encodes a seed-specific group A phosphatase 2C (PP2C) and is one of major negative regulators of seed dormancy among group A PP2Cs. Like other PP2C family members, HON interacts with PYR1/RCAR11 in the presence of abscisic acid (ABA). Our analysis indicates that HON inhibits ABA signaling and activates gibberellin (GA) signaling, and both of these conditions must be satisfied to promote the release of seed dormancy. However, HON mRNA levels are increased in mutants displaying deep seed dormancy or under conditions that deepen seed dormancy, and decreased in mutants displaying shallow seed dormancy or under conditions that promote the release of seed dormancy. Taken together, our results indicate that the expression of HON mRNA is homeostatically regulated by seed dormancy.
    Plant and Cell Physiology 02/2013; · 4.98 Impact Factor
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    ABSTRACT: Sugars enhance light signaling-induced anthocyanin accumulation in Arabidopsis seedlings via differential regulation of several positive and negative transcription factors. Ca(2+) plays a role as a second messenger in sugar signaling in grape and wheat. However, whether anthocyanin pigmentation is modulated by changes in intracellular Ca(2+) level in Arabidopsis is not known. Here, we used a pharmaceutical approach that Ca(2+) antagonists strongly interfered with sucrose uptake and anthocyanin accumulation by downregulating the expression of sucrose transporter 1 (SUC1) and transcriptional regulatory factors, such as PAP1. Time course analysis of the effect of Ca(2+) antagonists showed the early inhibition of sucrose-induced sugar uptake leading to decreased anthocyanin accumulation, indicating that Ca(2+) signals play a role in sugar uptake rather than in anthocyanin biosynthesis. An early increase in cytosolic Ca(2+) level in Arabidopsis roots in response to sucrose feeding was significantly inhibited by Ca(2+) antagonists. Taken together, these results indicate that sucrose-induced sugar uptake in Arabidopsis is modulated by changes in endogenous Ca(2+) levels, which in turn regulate anthocyanin accumulation.
    Biochemical and Biophysical Research Communications 12/2012; · 2.28 Impact Factor
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    ABSTRACT: Phytochromes are red and far-red light receptors in plants that mediate critical responses to light throughout the lifecycle. They achieve this in part by targeting negatively acting bHLH transcription factors called phytochrome-interacting factors (PIFs) for degradation within the nucleus. However, it is not known whether protein degradation is the primary mechanism by which phytochromes inhibit these repressors of photomorphogenesis. Here, we use chromatin immunoprecipitation to show that phyB inhibits the regulatory activity of PIF1 and PIF3 by releasing them from their DNA targets. The N-terminal fragment of phyB (NG-GUS-NLS; NGB) also inhibits binding of PIF3 to its target promoters. However, unlike full-length phyB, NGB does not promote PIF3 degradation, establishing the activity of NGB reflects its ability to inhibit PIF binding to DNA. We further show that Pfr forms of both full-length phyB and NGB inhibit DNA binding of PIF1 and PIF3 in vitro. Taken together, our results indicate that phyB inhibition of PIF function involves two separate processes: sequestration and protein degradation.
    The Plant Journal 07/2012; · 6.58 Impact Factor
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    ABSTRACT: In higher plants, the regulation of anthocyanin synthesis by various factors including light, sugars and hormones is mediated by numerous regulatory factors acting at the transcriptional level. Here, the association between sucrose and the plant hormone, cytokinin, in the presence of light was investigated to elucidate cytokinin signaling cascades leading to the transcriptional activation of anthocyanin biosynthesis genes in Arabidopsis seedlings. We showed that cytokinin enhances anthocyanin content and transcript levels of sugar inducible structural gene UDPglucose: flavonoid 3-O-glucosyl transferase (UF3GT) and regulatory gene PRODUCTION OF ANTHOCYANIN PIGMENT 1 (PAP1). Genetic analysis showed that cytokinin signaling modulates sugar-induced anthocyanin biosynthesis through a two-component signaling cascade involving the type-B response regulators ARR1, ARR10 and ARR12 in a redundant manner. Genetic, physiological and molecular biological approaches demonstrated that cytokinin enhancement is partially dependent on phytochrome and cryptochrome downstream component HY5, but mainly on photosynthetic electron transport. Taken together, we suggest that cytokinin acts down-stream of the photosynthetic electron transport chain in which the plastoquinone redox poise is modulated by sugars in a photoreceptor independent manner.
    Molecules and Cells 06/2012; 34(1):93-101. · 2.21 Impact Factor
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    ABSTRACT: Phytochromes (Phy) and phytochrome-interacting factor (PIF) transcription factors constitute a major signaling module that controls plant development in response to red and far-red light. A low red:far-red ratio is interpreted as shading by neighbor plants and induces cell elongation-a phenomenon called shade-avoidance syndrome (SAS). PAR1 and its closest homolog PAR2 are negative regulators of SAS; they belong to the HLH transcription factor family that lacks a typical basic domain required for DNA binding, and they are believed to regulate gene expressions through DNA binding transcription factors that are yet to be identified. Here, we show that light signal stabilizes PAR1 protein and PAR1 interacts with PIF4 and inhibits PIF4-mediated gene activation. DNA pull-down and chromatin immunoprecipitation (ChIP) assays showed that PAR1 inhibits PIF4 DNA binding in vitro and in vivo. Transgenic plants overexpressing PAR1 (PAR1OX) are insensitive to gibberellin (GA) or high temperature in hypocotyl elongation, similarly to the pifq mutant. In addition to PIF4, PAR1 also interacts with PRE1, a HLH transcription factor activated by brassinosteroid (BR) and GA. Overexpression of PRE1 largely suppressed the dwarf phenotype of PAR1OX. These results indicate that PAR1-PRE1 and PAR1-PIF4 heterodimers form a complex HLH/bHLH network regulating cell elongation and plant development in response to light and hormones.
    Molecular Plant 02/2012; 5(3):688-97. · 6.13 Impact Factor
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    Inyup Paik, Seungchan Yang, Giltsu Choi
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    ABSTRACT: An array of photoreceptors including cryptochromes, phototropin, and phytochromes regulates various light responses in plants. Among these photoreceptors, phytochromes perceive red and far-red light by switching between two interconvertible spectral forms (Pr and Pfr). The Pfr form promotes light responses partly by destabilizing negatively acting, phytochrome-interacting basic helix-loop-helix transcription factors (PIFs), thus modulating transcription in the nucleus. The Pfr form is also present in the cytosol. However, the role of phytochromes in the cytosol is not well understood. Here we show that the Pfr form interacts with the cytosolic protein PENTA1 (PNT1) and inhibits the translation of protochlorophyllide reductase (PORA) mRNA. PNT1 possesses five C3H-type zinc finger domains and displays similarity to various RNA binding proteins including Tristetraprolin, which regulates stabilities of mRNAs such as TNF-α mRNA in humans. Consistent with its function as an RNA binding protein, PNT1 directly binds to mRNA of a key chlorophyll biosynthetic gene, protochlorophyllide reductase in vivo and inhibits the translation of PORA mRNA in the presence of phytochromes. The present results demonstrate that phytochromes transmit light signals to regulate not only transcription in the nucleus through PIFs, but also translation in the cytosol through PNT1.
    Proceedings of the National Academy of Sciences 01/2012; 109(4):1335-40. · 9.81 Impact Factor
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    ABSTRACT: A previous study showed that SOMNUS (SOM), which encodes a C3H-type zinc finger protein, is a key negative regulator of seed germination that acts downstream of PHYTOCHROME INTERACTING FACTOR3-LIKE5 (PIL5). However, it was not determined if PIL5 is the sole regulator of SOM expression. Public microarray data suggest that the expression of SOM mRNA is regulated also by ABSCISIC ACID INSENSITIVE3 (ABI3), another key regulator of seed germination. By analyzing abi3 mutants and ABI3 overexpression lines, we show here that ABI3 activates the expression of SOM mRNA collaboratively with PIL5 in imbibed seeds. Chromatin immunoprecipitation analysis coupled with electrophoretic mobility shift assay indicate that ABI3 activates the expression of SOM mRNA by directly binding to two RY motifs present in the SOM promoter in vivo, which is further supported by the greatly decreased expression of a reporter gene driven by a SOM promoter bearing mutated RY motifs. At the protein level, the ABI3 protein interacts with the PIL5 protein. The ABI3-PIL5 interaction, however, does not affect targeting of ABI3 and PIL5 to SOM promoters. Taken together, our results indicate that ABI3 and PIL5 collaboratively activate the expression of SOM mRNA by directly binding to and interacting with each other at the SOM promoter.
    The Plant Cell 04/2011; 23(4):1404-15. · 9.25 Impact Factor
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    ABSTRACT: Phytochromes are red and far-red light photoreceptors that regulate various aspects of plant development. One of the less-understood roles of phytochromes is the inhibition of hypocotyl negative gravitropism, which refers to the loss of hypocotyl gravitropism and resulting random growth direction in red or far-red light. This light response allows seedlings to curve toward blue light after emergence from the soil and enhances seedling establishment in the presence of mulch. Phytochromes inhibit hypocotyl negative gravitropism by inhibiting four phytochrome-interacting factors (PIF1, PIF3, PIF4, PIF5), as shown by hypocotyl agravitropism of dark-grown pif1 pif3 pif4 pif5 quadruple mutants. We show that phytochromes inhibit negative gravitropism by converting starch-filled gravity-sensing endodermal amyloplasts to other plastids with chloroplastic or etioplastic features in red or far-red light, whereas PIFs promote negative gravitropism by inhibiting the conversion of endodermal amyloplasts to etioplasts in the dark. By analyzing transgenic plants expressing PIF1 with an endodermis-specific SCARECROW promoter, we further show that endodermal PIF1 is sufficient to inhibit the conversion of endodermal amyloplasts to etioplasts and hypocotyl negative gravitropism of the pif quadruple mutant in the dark. Although the functions of phytochromes in gravitropism and chloroplast development are normally considered distinct, our results indicate that these two functions are closely related.
    Proceedings of the National Academy of Sciences 01/2011; 108(4):1729-34. · 9.81 Impact Factor
  • Zhiyong Wang, Giltsu Choi
    Current opinion in plant biology 10/2010; 13(5):485-8. · 10.33 Impact Factor
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    ABSTRACT: Anthocyanin accumulation is regulated negatively by ethylene signaling and positively by sugar and light signaling. However, the antagonistic interactions underlying these signalings remain to be elucidated fully. We show that ethylene inhibits anthocyanin accumulation induced by sucrose (Suc) and light by suppressing the expression of transcription factors that positively regulate anthocyanin biosynthesis, including GLABRA3, TRANSPARENT TESTA8, and PRODUCTION OF ANTHOCYANIN PIGMENT1, while stimulating the concomitant expression of the negative R3-MYB regulator MYBL2. Genetic analyses show that the ethylene-mediated suppression of anthocyanin accumulation is dependent upon ethylene signaling components responsible for the triple response. Furthermore, these positive and negative signaling pathways appear to be under photosynthetic control. Suc and light induction of anthocyanin accumulation was almost fully inhibited in wild-type Arabidopsis (Arabidopsis thaliana) ecotype Columbia and ethylene (ethylene response1 [etr1-1]) and light (long hypocotyl1 [hy1], cryptochrome1/2, and hy5) signaling mutants treated with the photosynthetic electron transport inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea. The transcript level of the sugar transporter gene SUC1 was enhanced in ecotype Columbia treated with the ethylene-binding inhibitor silver and in etr1-1, ethylene insensitive2 (ein2-1), and ein3 ein3-like1 mutants. In contrast, 3-(3,4-dichlorophenyl)-1,1-dimethylurea treatment reduced SUC1 expression, which indicates strongly that SUC1 represents an integrator for signals provided by sugar, light, and ethylene. SUC1 mutations lowered accumulations of anthocyanin pigment, soluble sugar content, and ethylene production in response to Suc and light signals. These data demonstrate that the suppression of SUC1 expression by ethylene inhibits Suc-induced anthocyanin accumulation in the presence of light and, hence, fine-tunes anthocyanin homeostasis.
    Plant physiology 09/2010; 154(3):1514-31. · 6.56 Impact Factor
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    ABSTRACT: PIL5 is a member of the basic Helix-Loop-Helix (bHLH) transcription factor superfamily. We previously showed that PIL5 binds to the G-box (CACGTG) motif with high affinity. However, since there are many randomly matched G-box motifs throughout the genome, other factors must account for the in-vivo PIL5 binding specificity. In this study, we investigated if in-vivo PIL5 binding sites can be explained by any other attributes extracted from various sources. Our results showed that PIL5 binding sites can be explained by attributes such as neighbouring motif composition, nucleosome density, DNA methylation and distance from transcription start site in addition to G-box.
    International Journal of Data Mining and Bioinformatics 01/2010; 4(5):588-99. · 0.39 Impact Factor
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    ABSTRACT: Trimethylation of histone H3 at lysine 27 (H3K27me3) is a histone marker that is present in inactive gene loci in both plants and animals. Transcription of some of the genes with H3K27me3 should be induced by internal or external cues, yet the dynamic fate of H3K27me3 in these genes during transcriptional regulation is poorly understood in plants. Here we show that H3K27me3 in two cold-responsive genes, COR15A and ATGOLS3, decreases gradually in Arabidopsis during exposure to cold temperatures. We found that removal of H3K27me3 can occur by both histone occupancy-dependent and -independent mechanisms. Upon cold exposure, histone H3 levels decreased in the promoter regions of COR15A and ATGOLS3 but not in their transcribed regions. When we returned cold-exposed plants to normal growth conditions, transcription of COR15A and ATGOLS3 was completely repressed to the initial level before cold exposure in 1 day. In contrast, plants still maintained the cold-triggered decrease in H3K27me3 at COR15A and ATGOLS3, but this decrease did not enhance transcriptional induction of the two genes upon re-exposure to cold. Taken together, these results indicate that gene activation is not inhibited by H3K27me3 itself but rather leads to removal of H3K27me3, and that H3K27me3 can be inherited at a quantitative level, thereby serving as a memory marker for recent transcriptional activity in Arabidopsis.
    The Plant Journal 06/2009; 60(1):112-21. · 6.58 Impact Factor
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    ABSTRACT: PIF3 is a phytochrome-interacting basic helix-loop-helix transcription factor that negatively regulates light responses, including hypocotyl elongation, cotyledon opening, and hypocotyl negative gravitropism. However, the role of PIF3 in chlorophyll biosynthesis has not been clearly defined. Here, we show that PIF3 also negatively regulates chlorophyll biosynthesis by repressing biosynthetic genes in the dark. Consistent with the gene expression patterns, the etiolated pif3 mutant accumulated a higher amount of protochlorophyllide and was bleached severely when transferred into light. The photobleaching phenotype of pif3 could be suppressed by the gun5 mutation and mimicked by overexpression of GUN5. When 4 negative phytochrome-interacting protein genes (PIF1, PIF3, PIF4, and PIF5) were mutated, the resulting quadruple mutant seedlings displayed constitutive photomorphogenic phenotypes, including short hypocotyls, open cotyledons, and disrupted hypocotyl gravitropism in the dark. Microarray analysis further confirmed that the dark-grown quadruple mutant has a gene expression pattern similar to that of red light-grown WT. Together, our data indicate that 4 phytochrome-interacting proteins are required for skotomorphogenesis and phytochromes activate photomorphogenesis by inhibiting these factors.
    Proceedings of the National Academy of Sciences 05/2009; 106(18):7660-5. · 9.81 Impact Factor

Publication Stats

2k Citations
327.88 Total Impact Points

Institutions

  • 2010–2013
    • Chungnam National University
      • • College of Biological Sciences and Biotechnology
      • • Graduate School of Analytical Science and Technology
      Daiden, Daejeon, South Korea
    • Carnegie Institution for Science
      • Department of Plant Biology
      Washington, WV, United States
  • 2003–2013
    • Korea Advanced Institute of Science and Technology
      • Department of Biological Sciences
      Seoul, Seoul, South Korea
  • 2012
    • Kyoto University
      • Department of Botany
      Kioto, Kyōto, Japan
  • 2007
    • University of Missouri
      Columbia, Missouri, United States