| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online April 29, 2005; 10.1104/pp.104.058735 Plant Physiology 138:641-653 (2005) © 2005 American Society of Plant Biologists The Arabidopsis IspH Homolog Is Involved in the Plastid Nonmevalonate Pathway of Isoprenoid BiosynthesisDepartment of Genetics, Harvard Medical School, Boston, Massachusetts 02115 (M.H.H., H.M.G.); Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts 02114 (M.H.H., H.M.G.); and Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan (M.H.H.)
Plant isoprenoids are synthesized via two independent pathways, the cytosolic mevalonate (MVA) pathway and the plastid nonmevalonate pathway. The Escherichia coli IspH (LytB) protein is involved in the last step of the nonmevalonate pathway. We have isolated an Arabidopsis (Arabidopsis thaliana) ispH null mutant that has an albino phenotype and have generated Arabidopsis transgenic lines showing various albino patterns caused by IspH transgene-induced gene silencing. The initiation of albino phenotypes rendered by IspH gene silencing can arise independently from multiple sites of the same plant. After a spontaneous initiation, the albino phenotype is systemically spread toward younger tissues along the source-to-sink flow relative to the initiation site. The development of chloroplasts is severely impaired in the IspH-deficient albino tissues. Instead of thylakoids, mutant chloroplasts are filled with vesicles. Immunoblot analysis reveals that Arabidopsis IspH is a chloroplast stromal protein. Expression of Arabidopsis IspH complements the lethal phenotype of an E. coli ispH mutant. In 2-week-old Arabidopsis seedlings, the expression of 1-deoxy-D-xylulose 5-phosphate synthase (DXS), 1-deoxy-D-xylulose 5-phosphate reductoisomerase (DXR), IspD, IspE, IspF, and IspG genes is induced by light, whereas the expression of the IspH gene is constitutive. The addition of 3% sucrose in the media slightly increased levels of DXS, DXR, IspD, IspE, and IspF mRNA in the dark. In a 16-h-light/8-h-dark photoperiod, the accumulation of the IspH transcript oscillates with the highest levels detected in the early light period (2–6 h) and the late dark period (4–6 h). The expression patterns of DXS and IspG are similar to that of IspH, indicating that these genes are coordinately regulated in Arabidopsis when grown in a 16-h-light/8-h-dark photoperiod.
Isoprenoids are the largest group of natural products found in living organisms. Among the important isoprenoids are compounds such as steroid hormones in mammals, carotenoids and chlorophylls in plants, and ubiquinone or menaquinone in bacteria. Still others are medically important for human health, e.g. vitamins, hormones, and anticancer agents such as Taxol (Sacchettini and Poulter, 1997  ).
All isoprenoids are derived from a basic five-carbon unit, isopentenyl diphosphate (IPP), and its allyl isomer dimethylallyl diphosphate (DMAPP). For decades, the mevalonate (MVA) pathway was believed to be the only route to synthesize IPP and DMAPP. However, recent studies have uncovered an alternative nonmevalonate (nonMVA) pathway for isoprenoid biosynthesis (Rohmer et al., 1993
The nonMVA pathway has been found in a broad range of organisms, including bacteria, green algae, and higher plants (Eisenreich et al., 1998 , 2001; Lichtenthaler, 1999; Cunningham et al., 2000; Rohdich et al., 2001; Rodriguez-Concepcion and Boronat, 2002). In plants, the MVA and nonMVA pathways are compartmentalized in the cytoplasm and plastid, respectively. Sesquiterpenes, sterols, and polyterpenes are derived from the cytosolic MVA pathway, whereas isoprene, phytol, carotenoids, and plant hormones GA and abscisic acid are synthesized via the plastid nonMVA pathway (Fig. 1). The Arabidopsis genome contains genes encoding homologs of E. coli nonMVA pathway enzymes and the deduced amino acid sequences all possess a transit peptide for chloroplast localization, consistent with their predicted role in the biosynthesis of plastid isoprenoids (Rodriguez-Concepcion and Boronat, 2002).
Previous studies have shown that Arabidopsis plants (cla1-1 mutants) with a null mutation in the DXS gene are albino (Mandel et al., 1996 To isolate plant nonMVA pathway mutants, we generated Arabidopsis T-DNA insertion lines and screened for plants showing pale green or albino phenotypes. One of the isolated Arabidopsis albino mutants is caused by a T-DNA insertion in a gene that encodes a protein with significant similarity to E. coli IspH (or LytB). Consistent with the albino phenotype observed in the null mutant, Arabidopsis IspH gene-silencing plants show pale green to various albino patterns. Levels of IspH mRNA are dramatically reduced in the IspH-silenced albino tissues. We also provide experimental evidence that the Arabidopsis IspH protein is localized in the chloroplast stroma. A complementation test with an E. coli ispH mutant further confirms that the Arabidopsis IspH protein functions as a nonMVA pathway enzyme involved in the biosynthesis of plastid isoprenoids.
The biosynthesis of plastid isoprenoids is directly linked to photosynthesis. We have thus examined the effects of light and Suc on the expression of nonMVA pathway genes in Arabidopsis. In addition, it has been suggested that the biosynthesis and emission of volatile plant isoprenoids are derived from the plastid nonMVA pathway (Lichtenthaler, 1999
Phenotypic Analysis of the Arabidopsis ispH-1 Mutant We isolated the albino ispH-1 mutant by screening a collection of Arabidopsis T-DNA insertion lines. Genetic analysis and thermal asymmetric interlaced-PCR revealed that the albino line 3a234 contains two copies of T-DNA in two different loci, IspH and At3g46440, which were further segregated as two different lines. Homozygous ispH-1 plants are albino and progeny from a self-pollinated heterozygous plant segregate green and albino plants in a 3:1 ratio on a nonselective medium, i.e. the albino phenotype is inherited as a recessive mutation (Fig. 2A). The ispH-1 mutant seedlings exhibit a purple-tinted phenotype superimposed on the albino phenotype when grown on the medium containing Suc (Fig. 2A). The purple coloration begins to fade about 1 week after germination on this medium. The ispH-1 albino plant can develop a normal root system, rosette leaves, an inflorescence with cauline leaves, and flower-like structures that never mature into normal flowers when grown on tissue culture medium (Fig. 2B).
To study the effect of the ispH-1 mutation on chloroplast development, leaf sections of Arabidopsis wild-type and ispH-1 plants were examined by transmission electron microscopy. In contrast to the lens-shaped wild-type chloroplast (Fig. 2C), the ispH-1 mutant chloroplasts are usually round, oval, or irregularly shaped (Fig. 2D; data not shown). In addition, the mutant chloroplasts completely lack thylakoids and contain large vesicles (Fig. 2D). In ispH-1 mutants, total chlorophylls and carotenoids are less than 1% and 2%, respectively, of their amounts in the wild type (Table I).
Molecular Characterization and Complementation of the ispH-1 Locus Analysis of the flanking genomic DNA sequences revealed that the Arabidopsis ispH-1 mutant has a T-DNA insertion in the seventh exon of the IspH gene (Fig. 3A). Northern and immunoblot analyses showed that the IspH mRNA and protein were undetectable in the ispH-1 mutant (Fig. 3B). These results suggest that ispH-1 is a null mutant. In 6-week-old wild-type Arabidopsis plants, the IspH transcript was detected in all tissues analyzed (Fig. 3C). To prove that the defective ispH-1 locus is responsible for the albino phenotype, we restored the wild-type phenotype by introducing into the mutant a full-length IspH cDNA transcribed from a cauliflower mosaic virus 35S promoter. The phenotype of a representative complementation line is shown in Figure 3D. Genomic DNA-blot analysis was used to verify that the complemented plants contained a (homozygous) ispH-1 mutant allele and a 35S:IspH transgene (Fig. 3E). These results confirm that the albino phenotype is caused by disruption of the IspH gene.
Arabidopsis 35S:IspH cDNA Transgene-Induced Gene Silencing
Attempts to create Arabidopsis IspH overexpression lines resulted in some primary transformants showing pale green or various albino phenotypes (Fig. 4, A and B). In plants, some transgenes may cause a coordinated silencing of the transgene and homologous host genes (Mlotshwa et al., 2002
Initiation and Systemic Spread of IspH Gene Silencing The visual albino phenotype that is a result of IspH gene silencing serves as a marker for observing the initiation and systemic spread of transgene-induced gene silencing in Arabidopsis. The initiation of IspH gene silencing is spontaneous and stochastic; it may arise at various developmental stages and several independent initiations may even occur in the same plant. For instance, the albino phenotype may appear independently in rosette leaves, stems, and siliques (Fig. 5A). After the initiation step, somehow the IspH gene-silencing signal(s) is systemically spread toward developing tissues so that younger tissues that develop above the initiation site will be affected (Fig. 5, A–C). Expanding cauline leaves, at the time of initiation, either are not or are only partially affected, leading to a phenotype where a green leaf and a partially green leaf are attached to an albino stem (Fig. 5D). Sometimes the apical region of a silenced inflorescence may remain green, which indicates that the IspH gene is not always silenced in the meristematic regions (Fig. 5, A, D, and L). In siliques, IspH gene silencing can be localized in the base, in the tip, in the middle, or at both ends independently and gradually spreads throughout the entire silique (Fig. 5, A, D, and E). The random initiation and systemic spread of the albino phenotype in siliques indicate that cells in developing siliques may not have a distinct source-to-sink status for silencing signals as in leaves or stems. In T3 homozygous lines, the mixed progeny of nonsilenced (green) and silenced plants with various albino patterns segregate randomly (Fig. 5F).
When the initiation of IspH gene silencing is localized in rosette leaves during the vegetative stage, leaves that have expanded before the initiation will not be affected (Fig. 5, G–I). If the initiation occurs in rosette leaves during the transition from vegetative to reproductive stage, the green inflorescence tip has a chance to develop flowers and siliques before the entire inflorescence becomes albino (Fig. 5, J–L). Neither initiation nor systemic spread of IspH gene silencing was observed in fully expanded rosette leaves.
In a partially silenced rosette leaf, chloroplasts in the green cells accumulate more starch granules than the comparable wild type (Fig. 6, A and B), whereas in the IspH-silenced albino tissue, chloroplasts are highly vesiculated (Fig. 6C). Because the basal part of an expanding leaf is composed of younger tissues, it is possible that these vesicles are derived from undifferentiated chloroplasts. During the systemic spread of IspH gene silencing in a leaf, a narrow boundary line of pale green to pale yellow forms between the green and the albino tissue. Transmission electron microscopy reveals that various types of chloroplasts exist in this region (Fig. 6, D–I). Chloroplasts of pale green tissues close to the nonsilenced green part of the leaf have highly differentiated thylakoids, but most of the stroma lamellae are discontinuous and stacked thylakoids are thicker than the wild type (Fig. 6D). By contrast, chloroplasts of pale yellow tissues close to the albino part of the leaf have only a few differentiated thylakoids (Fig. 6, E and F), mixed vesicles and loosening thylakoids (Fig. 6G), small vesicles (Fig. 6H), or large vesicles (Fig. 6I). The IspH-silencing chloroplasts also contain densely stained globule (lipid-droplet) aggregates (Fig. 6, D, E, G, and I). Since the systemic spread of the albino phenotype starts from the initiation site toward developing tissues, these chloroplasts may represent a broad range of undifferentiated, partially differentiated, and fully differentiated chloroplasts that are affected by photooxidation caused by various levels of IspH gene silencing. The vesicular structures and densely stained globule aggregates observed in these chloroplasts may be derived from the precursor components or breakdown products of thylakoids.
Arabidopsis IspH Is a Chloroplast Stromal Protein
Alignment of IspH amino acid sequences from plants (Arabidopsis and Adonis), cyanobacterium, and E. coli indicates that both plant IspH proteins have an extra N-terminal sequence with the features of a chloroplast transit peptide (data not shown; Botella-Pavia et al., 2004
Arabidopsis IspH Complements the E. coli ispH Mutant
To test whether the Arabidopsis IspH protein has similar enzymatic activity to its E. coli counterpart, we performed a complementation assay with an E. coli ispH mutant. In E. coli ispH mutant strain MG1655 ara<>ispH, the endogenous IspH gene was replaced by a kanamycin-resistant cassette and a single copy of IspH was present on the chromosome under the control of the PBAD promoter (McAteer et al., 2001
Light Induction of the nonMVA Pathway Genes
It has been shown that expression of Arabidopsis DXS and DXR (IspC) genes is induced by light (Mandel et al., 1996
Expression Patterns of the nonMVA Pathway Genes in a Normal Day/Night Cycle
To further investigate whether expression of the nonMVA pathway genes is coordinately regulated, we compared the day/night expression patterns of these genes in 13- and 14-d-old Arabidopsis seedlings (Fig. 10). Interestingly, several distinct diurnal expression patterns were observed in the Arabidopsis nonMVA pathway genes. The expression patterns of DXS, IspG, and IspH are similar during the 16-h-light/8-h-dark cycle. Peak levels of DXS, IspG, and IspH mRNA were detected in the early period of the light cycle (2–6 h in the light) and in the late period of the dark cycle (6–8 h in the dark). An additional peak appeared at the end of the light cycle (16 h), which is more evident in relative mRNA levels of DXS and IspG and less obvious in that of IspH (Fig. 10B). Oscillations in DXR, IspD, IspE, and IspF mRNA accumulation also occurred during the light/dark cycle. In contrast to DXS, IspG, and IspH, peak levels of IspD mRNA appeared in the late period of the light cycle (12–16 h). The highest levels of DXR, IspE, and IspF mRNA were also detected in the late period (14 h) of the light cycle. An additional peak in the early period (2–6 h) of the light cycle is evident in the relative mRNA levels of IspE and less obvious in those of DXR and IspF. Interestingly, the expression of all nonMVA pathway genes is significantly repressed during the transition from light to dark (Fig. 10; compare light 16 h to dark 2 h in each cycle). The same RNA samples were used to detect the light/dark expression patterns of Arabidopsis ASN1 (encoding Asn synthetase) and rbcS (encoding Rubisco small subunit) as controls. The expression of Arabidopsis ASN1 is induced by dark and repressed by light (Lam et al., 1998
The E. coli LytB protein was originally identified as one of the components involved in penicillin tolerance and control of the stringent response (Gustafson et al., 1993 ). Studies on a lytB mutant of the cyanobacterium Synechocystis strain PCC 6803 provided evidence of a role for LytB in the nonMVA pathway of isoprenoid biosynthesis (Cunningham et al., 2000). Mutagenesis studies in E. coli also suggested that the LytB protein is involved in the nonMVA pathway (Altincicek et al., 2001; McAteer et al., 2001). Recent in vivo and in vitro experiments have confirmed that E. coli LytB catalyzes the last reaction of the nonMVA pathway, a branching step that separately produces IPP and DMAPP in a ratio of 5:1 to 6:1 (Adam et al., 2002; Altincicek et al., 2002; Rohdich et al., 2002, 2003). E. coli LytB was thus renamed IspH (Adam et al., 2002).
Here, we report the identification and characterization of an Arabidopsis albino mutant that has a null mutation in the IspH gene. The phenotype of the ispH-1 mutant and the IspH gene-silencing lines and the localization of the IspH protein are in accord with a role for Arabidopsis IspH in plastid isoprenoid biosynthesis. Consistent with our studies, Page et al. (2004)
The phenomenon of transgene-induced gene silencing was first uncovered as coordinate silencing (cosuppression) of both the transgene and the homologous plant gene in petunia (Napoli et al., 1990
The systemic spread of the IspH-silenced albino phenotype toward younger developing tissues, including the apical meristem (Fig. 5, A, C, and G–L), suggests that the transmission of IspH-silencing signals is unidirectional and of high efficiency. In addition, there is no obvious temporal difference in the appearance of albino phenotypes between vein and nonvein tissues during the spread of IspH gene silencing (Fig. 5, G–L). The resulting IspH-silenced tissues are uniformly photobleached rather than variegated. The direction of systemic spread of IspH gene silencing parallels the flow of metabolic source to sink in leaves and stems. In siliques, however, the spread of silencing signals is stochastic (Fig. 5E). The processes involved in carpel and fruit development are not well understood in Arabidopsis (Ferrándiz et al., 1999
Taking advantage of the systemic spread of the albino phenotype from the initiation site toward developing tissues, we have observed a series of morphological changes in the chloroplasts of IspH gene-silencing cells (Fig. 6, D–I). The integration of the LHCs, which are mainly composed of chlorophylls, carotenoids, and apoproteins, is important for the development of thylakoids and the formation of grana stacking (Bartley and Scolnik, 1995
Although Arabidopsis IspH only shares about 24% identity (approximately 40% similarity) with the E. coli protein at the amino acid level, expression of Arabidopsis IspH complements the E. coli ispH mutant (Fig. 8). The E. coli IspH protein is a reductase that possesses a dioxygen-sensitive [4Fe-4S] cluster (Wolff et al., 2003
In addition to functional analysis and subcellular localization of the Arabidopsis IspH protein, we also characterized the expression and regulation of the Arabidopsis IspH gene. The Arabidopsis IspH transcripts are detected in all parts of adult plants, indicating that the IspH protein has an essential function throughout the entire plant (Fig. 3C). The expression of the Arabidopsis IspH gene in both photosynthetic and nonphotosynthetic tissues supports the notion that the nonMVA pathway is involved in synthesizing a variety of isoprenoids in plants. Consistent with their roles in synthesizing carotenoids and chlorophylls for photosynthesis, the Arabidopsis nonMVA pathway genes are highly expressed in light and most are low in the dark (Fig. 9). The only exception is the IspH gene, whose expression is constitutive regardless of the continuous light/dark treatments in 2-week-old Arabidopsis plants. Interestingly, it has been shown that the expression of the IspH gene is up-regulated during Arabidopsis seedling deetiolation and levels of Arabidopsis IspH mRNA are significantly higher in 3-d-old seedlings grown in continuous light than those of dark-grown seedlings (Botella-Pavia et al., 2004 Since the initial substrates of the nonMVA pathway, pyruvate and glyceraldehyde 3-phosphate, may directly derive from glycolysis and photosynthesis in the chloroplast, carbon metabolites may affect the expression of the nonMVA pathway genes. We have found that the expression of the DXS, DXR, IspD, IspE, and IspF genes is slightly induced by Suc in the dark, whereas the presence of Suc in the light has no additive effects beyond the light induction of the nonMVA pathway genes. These results suggest that at least some of the Arabidopsis nonMVA pathway genes are subjected to metabolic regulation.
Although the expression of the IspH gene is not affected by prolonged (48-h) light or dark treatment (Fig. 9), levels of IspH mRNA oscillate during a 16-h-light/8-h-dark cycle in 2-week-old Arabidopsis plants (Fig. 10). Among the nonMVA pathway genes, DXS and IspG share the most similar expression patterns with IspH during a normal light/dark cycle. Interestingly, expression of the Arabidopsis DXS and IspH genes is coordinately regulated during deetiolation (Botella-Pavia et al., 2004
The MVA pathway in animal cells is regulated at multiple levels, including transcriptional, posttranscriptional, and a complex feedback regulatory system (Goldstein and Brown, 1990
The existence of two independent IPP biosynthetic pathways inside a plant cell raises an interesting question as to whether and, if so, how these two pathways interact with each other. It has been suggested that interactions between the cytosolic MVA pathway and the plastid nonMVA pathway may exist in plants (Eisenreich et al., 1998
Nomenclature
The nonMVA or MVA-independent pathway has also been called the DXP pathway or the MEP pathway in the literature (Eisenreich et al., 1998
Arabidopsis (Arabidopsis thaliana ecotype Columbia-0) was grown on half-strength Murashige and Skoog plates (Murashige and Skoog salts [GIBCO/BRL, Cleveland], pH adjusted to 5.7 with 1 N KOH, 0.8% [w/v] phytoagar) containing 2% Suc, or in soil in the greenhouse on a 16-h-light/8-h-dark cycle at 23°C. For experiments in which plants were transferred to 0% Suc, 3% Suc, or 3% mannitol (Fig. 9), seeds were sown on 1.5- x 8-cm nylon nets with 250-µm mesh size (Tetko, Elmsford, NY; catalog no. 3–250/50) placed on the surface of the media. For transfer to new media, the nylon nets were lifted, and the plants were transferred to fresh Murashige and Skoog media containing the indicated supplementations. Determination of total chlorophyll and carotenoids in three independent samples of 2-week-old Arabidopsis wild-type and ispH-1 seedlings grown in tissue culture was conducted as described (Linchtenhaler and Wellburn, 1983
A binary vector pBI121 with a kanamycin-selectable marker was transformed into Arabidopsis ecotype Columbia-0 to generate a collection of approximately 4,000 T-DNA lines. T2 seeds of each independent T-DNA line were used to screen for albino mutants. Thermal asymmetric interlaced-PCR was used to determine the T-DNA flanking genomic sequences of these mutants (Liu et al., 1995
Total RNA from 2-week-old Arabidopsis was used for reverse transcription-PCR (SuperScriptII reverse transcriptase kit; Invitrogen, Carlsbad, CA), and primers 5'-GTGCGTTTCTCTCGAACTCT-3' and 5'-GGTAAGAACATTAAGTGGAG-3' were used to amplify a full-length IspH cDNA. The PCR product was cloned into pCR2.1-TOPO (Invitrogen) and provided for sequencing. The Arabidopsis IspH cDNA sequence and the deduced amino acid sequence were deposited in GenBank (AY168881).
The full-length IspH cDNA driven by a cauliflower mosaic virus 35S promoter in the sense orientation was subcloned into a plant expression vector pSMAB704 containing the basta resistance (BAR) selectable marker and transformed by floral dip (Clough and Bent, 1998
Arabidopsis total RNA was isolated using a phenol extraction protocol (Jackson and Larkins, 1976
The leaf samples were fixed in 4% glutaraldehyde, 100 mM sodium cacodylate, pH 7.2, for 16 h at 4°C, and postfixed with 1% osmium tetroxide in the same buffer for 6 h at 4°C. The fixed samples were dehydrated through a series of alcohol solutions and embedded in Spurr resin. Ultrathin sections were cut on a Reichert Ultracut-S (Leica Microsystems, Bannockburn, IL) and stained with uranyl acetate and lead citrate and viewed with a transmission electron microscope, JEOL 1200EX (JEOL USA, Peabody, MA).
The Arabidopsis IspH cDNA was digested with SacI and BamHI and cloned into similarly cut pQE-30 (Qiagen, Valencia, CA) to express His-tagged IspH protein in Escherichia coli. The resulting clone, pQE-AtIspH, encodes a nearly complete mature Arabidopsis IspH protein missing the first 24 amino acid residues with a 6x His tag at the N terminus. Purification of the His-tagged IspH protein was performed according to The QIAexpressionist, fourth edition (Qiagen). Polyclonal antibodies were raised by immunization of a rabbit using the purified fusion protein (Cocalico Biologicals, Reamstown, PA). Total protein extraction, chloroplast isolation, and immunoblot analysis were performed as described (Hsieh et al., 1998
The E. coli ispH mutant strain MG1655 ara<>ispH was maintained on Luria-Bertani medium containing 50 µg/mL kanamycin and 0.2% (w/v) Ara (McAteer et al., 2001 Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession number AY168881.
We thank Dr. J. Sheen for the pSMAB704 binary vector and OE33, LHCII, and rbcS polyclonal antibodies, and Dr. M. Masters for the E. coli ispH mutant strain. Received December 21, 2004; returned for revision February 26, 2005; accepted February 27, 2005.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.058735. * Corresponding author; e-mail ming{at}gate.sinica.edu.tw; fax 886–2–2782–7954.
Adam P, Hecht S, Eisenreich W, Kaiser J, Grawert T, Arigoni D, Bacher A, Rohdich F (2002) Biosynthesis of terpenes: studies on 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase. Proc Natl Acad Sci USA 99: 12108–12113 Altincicek B, Duin EC, Reichenberg A, Hedderich R, Kollas AK, Hintz M, Wagner S, Wiesner J, Beck E, Jomaa H (2002) LytB protein catalyzes the terminal step of the 2-C-methyl-D-erythritol-4-phosphate pathway of isoprenoid biosynthesis. FEBS Lett 532: 437–440[CrossRef][Medline] Altincicek B, Kollas A, Eberl M, Wiesner J, Sanderbrand S, Hintz M, Beck F, Jomaa H (2001) LytB, a novel gene of the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli. FEBS Lett 499: 37–40[CrossRef][Web of Science][Medline] Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7: 1027–1038[CrossRef][Web of Science][Medline] Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415: 146–154[Medline] Botella-Pavia P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodriguez-Concepcion M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40: 188–199[CrossRef][Web of Science][Medline]
Budziszewski GJ, Lewis SP, Glover LW, Reineke J, Jones G, Ziemnik LS, Lonowski J, Nyfeler B, Aux G, Zhou Q, et al (2001) Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning. Genetics 159: 1765–1778
Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A, Campos N (2002) Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-D-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Plant Physiol 129: 1581–1591 Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743[CrossRef][Web of Science][Medline]
Cunningham FX Jr, Lafond TP, Gantt E (2000) Evidence of a role for LytB in the nonmevalonate pathway of isoprenoid biosynthesis. J Bacteriol 182: 5841–5848 De Carvalho F, Gheysen G, Kushnir S, Van Montagu M, Inze D, Castresana C (1992) Suppression of beta-1,3-glucanase transgene expression in homozygous plants. EMBO J 11: 2595–2602[Web of Science][Medline] Dedonder A, Rethy R, Fredericq H, Van Montagu M, Krebbers E (1993) Arabidopsis rbcS genes are differentially regulated by light. Plant Physiol 101: 801–808[Abstract]
Dormann P, Balbo I, Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284: 2181–2184
Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Faldt J, Miller B, Bohlman J (2003) (E)- Eisenreich W, Rohdich F, Bacher A (2001) Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci 6: 78–84[CrossRef][Web of Science][Medline] Eisenreich W, Schwarz M, Cartayrade A, Arigoni D, Zenk MH, Bacher A (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem Biol 5: R221–R233[CrossRef][Medline]
Estevez JM, Cantero A, Reindl A, Reichler S, Leon P (2001) 1-Deoxyxylulose 5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276: 22901–22909
Estevez JM, Cantero A, Romero C, Kawaide H, Jimenez LF, Kuzuyama T, Seto H, Kamiya Y, Leon P (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124: 95–103 Fagard M, Vaucheret H (2000) (Trans)gene silencing in plants: how many mechanisms? Annu Rev Plant Physiol Plant Mol Biol 51: 167–194[CrossRef][Web of Science]
Feinberg EH, Hunter CP (2003) Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301: 1545–1547 Ferrándiz C, Pelaz S, Yanofsky MF (1999) Control of carpel and fruit development in Arabidopsis. Annu Rev Biochem 68: 321–354[CrossRef][Web of Science][Medline] Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811[CrossRef][Medline] Goldstein JL, Brown M (1990) Regulation of the mevalonate pathway. Nature 343: 425–430[CrossRef][Medline]
Guevara-Garcia A, San Roman C, Arroyo A, Cortes ME, de la Luz Gutierrez-Nava M, Leon P (2005) Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-D-erythritol 4-phosphate pathway. Plant Cell 17: 628–643
Gustafson CE, Kaul S, Ishiguro EE (1993) Identification of the Escherichia coli lytB gene, which is involved in penicillin tolerance and control of the stringent response. J Bacteriol 175: 1203–1205
Gutierrez-Nava M de L, Gillmor CS, Jimenez LF, Guevara-Garcia A, Leon P (2004) CHLOROPLAST BIOGENESIS genes act cell and noncell autonomously in early chloroplast development. Plant Physiol 135: 471–482 Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671–4679[CrossRef][Web of Science][Medline]
Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950–952
Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110–2113
Hecht S, Eisenreich W, Adam P, Amslinger S, Kis K, Bacher A, Arigoni D, Rohdich F (2001) Studies on the nonmevalonate pathway to terpenes: the role of the GcpE (IspG) protein. Proc Natl Acad Sci USA 98: 14837–14842
Herz S, Wungsintaweekul J, Schuhr CA, Hecht S, Luttgen H, Sagner S, Fellermeier M, Eisenreich W, Zenk MH, Bacher A, et al (2000) Biosynthesis of terpenoids: YgbB protein converts 4-diphosphocytidyl-2C-methyl-D-erythritol 2-phosphate to 2C-methyl-D-erythritol 2,4-cyclodiphosphate. Proc Natl Acad Sci USA 97: 2486–2490 Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22: 4523–4533[CrossRef][Web of Science][Medline] Hsieh MH (1998) Metabolic regulation of asparagine synthetase genes and characterization of a putative nitrogen sensor (PII) in Arabidopsis. PhD thesis. New York University, New York
Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G (1998) A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc Natl Acad Sci USA 95: 13965–13970
Jackson AO, Larkins BA (1976) Influence of ionic strength, pH, and chelation of divalent metals on isolation of polyribosomes from tobacco leaves. Plant Physiol 57: 5–10
Jorgensen RA, Atkinson RG, Forster RLS, Lucas WJ (1998) An RNA-based information superhighway in plants. Science 279: 1486–1487
Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277: 45188–45194
Klahre U, Crete P, Leuenberger SA, Iglesias VA, Meins F (2002) High molecular weight RNAs and small interfering RNAs induce systemic posttranscriptional gene silencing in plants. Proc Natl Acad Sci USA 99: 11981–11986
Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13: 2333–2347 Lam HM, Hsieh MH, Coruzzi G (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J 16: 345–353[CrossRef][Web of Science][Medline]
Laule O, Furholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6866–6871 Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid synthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50: 47–65[CrossRef][Web of Science] Linchtenhaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11: 591–592 Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junction by thermal asymmetric interlaced PCR. Plant J 8: 457–463[CrossRef][Web of Science][Medline]
Lois LM, Campos N, Putra SR, Danielsen K, Rohmer M, Boronat A (1998) Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proc Natl Acad Sci USA 95: 2105–2110
Loreto F, Ciccioli P, Brancaleoni E, Cecinato A, Frattoni M, Sharkey T (1996) Different sources of reduced carbon contribute to form three classes of terpenoid emitted by Quercus ilex L. leaves. Proc Natl Acad Sci USA 93: 9966–9969
Lu S, Xu R, Jia JW, Pang J, Matsuda SP, Chen XY (2002) Cloning and functional characterization of a beta-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol 130: 477–486 Lucas WJ, Yoo B-C, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2: 849–857[CrossRef][Web of Science][Medline]
Luttgen H, Rohdich F, Herz S, Wungsintaweekul J, Hecht S, Schuhr CA, Fellermeier M, Sagner S, Zenk MH, Bacher A, et al (2000) Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-diphosphocytidyl-2C-methyl-D-erythritol. Proc Natl Acad Sci USA 97: 1062–1067 Mallory AC, Mlotshwa S, Bowman LH, Vance VB (2003) The capacity of transgenic tobacco to send a systemic RNA silencing signal depends on the nature of the inducing transgene locus. Plant J 35: 82–92[CrossRef][Web of Science][Medline] Mandel MA, Feldmann KA, Herrera-Estrella L, Rocha-Sosa M, Leon P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9: 649–658[CrossRef][Web of Science][Medline]
Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132: 1586–1599
McAteer S, Coulson A, McLennan N, Masters M (2001) The lytB gene of Escherichia coli is essential and specifies a product needed for isoprenoid biosynthesis. J Bacteriol 183: 7403–7407 Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB (2002) RNA silencing and the mobile silencing signal. Plant Cell (Suppl) 14: S289–S301 Myerson D (1991) Producing single-stranded DNA probes with the Taq DNA polymerase: a high yield protocol. Biotechniques 10: 35–38[Medline] Nagata N, Suzuki M, Yoshida S, Muranaka T (2002) Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the nonmevalonate pathway. Planta 216: 345–350[CrossRef][Web of Science][Medline]
Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible cosuppression of homologous genes in trans. Plant Cell 2: 279–289 Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333–359[CrossRef][Web of Science] Okada K, Kawaide H, Kuzuyama T, Seto H, Curtis IS, Kamiya Y (2002) Antisense and chemical suppression of the nonmevalonate pathway affects ent-kaurene biosynthesis in Arabidopsis. Planta 215: 339–344[CrossRef][Web of Science][Medline]
Page JE, Hause G, Raschke M, Gao W, Schmidt J, Zenk MH, Kutchan TM (2004) Functional analysis of the final steps of the 1-deoxy-D-xylulose 5-phosphate (DXP) pathway to isoprenoids in plants using virus-induced gene silencing. Plant Physiol 134: 1401–1413 Palauqui J-C, Elmayan T, Pollien J-M, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16: 4738–4745[CrossRef][Web of Science][Medline] Pilgrim ML, McClung CR (1993) Differential involvement of the circadian clock in the expression of genes required for ribulose-1,5-bisphosphate carboxylase/oxygenase synthesis, assembly, and activation in Arabidopsis thaliana. Plant Physiol 103: 553–564[Abstract]
Rodriguez-Concepcion M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130: 1079–1089
Rohdich F, Hecht S, Gartner K, Adam P, Krieger C, Amslinger S, Arigoni D, Bacher A, Eisenreich W (2002) Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc Natl Acad Sci USA 99: 1158–1163 Rohdich F, Kis K, Bacher A, Eisenreich W (2001) The non-mevalonate pathway of isoprenoids: genes, enzymes and intermediates. Curr Opin Chem Biol 5: 535–540[CrossRef][Web of Science][Medline]
Rohdich F, Wungsintaweekul J, Fellermeier M, Sagner S, Herz S, Kis K, Eisenreich W, Bacher A, Zenk MH (1999) Cytidine 5'-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2-C-methylerythritol. Proc Natl Acad Sci USA 96: 11758–11763
Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Grawert T, Amslinger S, Eisenreich W, Bacher A, et al (2003) The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc Natl Acad Sci USA 100: 1586–1591 Rohmer M (2003) Mevalonate-independent methylerythritol phosphate pathway for isoprenoid biosynthesis: elucidation and distribution. Pure Appl Chem 75: 375–388 Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295: 517–524
Sacchettini JC, Poulter CD (1997) Creating isoprenoid diversity. Science 277: 1788–1789
Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13: 113–123 Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52: 407–436[CrossRef][Web of Science][Medline]
Simidjiev I, Stoylova S, Amenitsch H, Javorfi T, Mustardy L, Laggner P, Holzenburg A, Garab G (2000) Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro. Proc Natl Acad Sci USA 97: 1473–1476
Sprenger GA, Schorken U, Wiegert T, Grolle S, de Graaf AA, Taylor SV, Begley TP, Bringer-Meyer S, Sahm H (1997) Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-D-xylulose 5-phosphate precursor to isoprenoids, thiamin, and pyridoxol. Proc Natl Acad Sci USA 94: 12857–12862
Takahashi S, Kuzuyama T, Watanabe H, Seto H (1998) A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc Natl Acad Sci USA 95: 9879–9884 Van Blokland R, van der Geest N, Mol J, Kooter J (1994) Transgene-mediated suppression of chalcone synthase expression in Petunia hybrida results from an increase in RNA turnover. Plant J 6: 861–877[CrossRef][Web of Science]
Vance V, Vaucheret H (2001) RNA silencing in plants—defense and counterdefense. Science 292: 2277–2280
Van der Krol A, Mur L, Beld M, Mol JNM, Stuitje AR (1990) Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2: 291–299
Vaucheret H, Beclin C, Fagard M (2001) Post-transcriptional gene silencing in plants. J Cell Sci 114: 3083–3091 Voinnet O, Vain P, Angell S, Baulcombe DC (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177–187[CrossRef][Web of Science][Medline] Von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7: 1039–1057[CrossRef][Web of Science][Medline] Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541: 91–101[Medline] White RH (1978) Stable isotope studies on the biosynthesis of the thiazole moiety of thiamin in Escherichia coli. Biochemistry 17: 3833–3840[CrossRef][Medline]
Winston WM, Molodowitch C, Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295: 2456–2459 Wolff M, Seemann M, Tse BSB, Frapart Y, Tritsch D, Estrabot AG, Rodriguez-Concepcion M, Boronat A, Marquet A, Rohmer M (2003) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe-4S] protein. FEBS Lett 541: 115–120[CrossRef][Medline]
Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ (2004) A systemic small RNA signaling system in plants. Plant Cell 16: 1979–2000 Zeidler J, Lichtenthaler HK (2001) Biosynthesis of 2-methyl-3-buten-2-ol emitted from needles of Pinus ponderosa via the non-mevalonate DOXP/MEP pathway of isoprenoid formation. Planta 213: 323–326[Medline] This article has been cited by other articles:
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
-Ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new TPS-subfamily. Plant Cell 15: 1227–1241
