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First published online June 12, 2003; 10.1104/pp.103.021022 Plant Physiology 132:1260-1271 (2003) © 2003 American Society of Plant Biologists Phosphate Starvation Triggers Distinct Alterations of Genome Expression in Arabidopsis Roots and Leaves1,[w]State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, 310029, China (P.W., X.H., M.W., Y.W., F.L.); Peking-Yale Joint Center of Plant Molecular Genetics and Agrobiotechnology, College of Life Sciences, Peking University, Beijing 100871, Peoples Republic of China (L.M., X.W.D.); and Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520–8104 (L.M., X.W.D.)
Arabidopsis genome expression pattern changes in response to phosphate (Pi) starvation were examined during a 3-d period after removal of Pi from the growth medium. Available Pi concentration was decreased after the first 24 h of Pi starvation in roots by about 22%, followed by a slow recovery during the 2nd and 3rd d after Pi starvation, but no significant change was observed in leaves within the 3 d of Pi starvation. Microarray analysis revealed that more than 1,800 of the 6,172 genes present in the array were regulated by 2-fold or more within 72 h from the onset of Pi starvation. Analysis of these Pi starvation-responsive genes shows that they belong to wide range of functional categories. Many genes for photosynthesis and nitrogen assimilation were down-regulated. A complex set of metabolic adaptations appears to occur during Pi starvation. More than 100 genes each for transcription factors and cell-signaling proteins were regulated in response to Pi starvation, implying major regulatory changes in cellular growth and development. A significant fraction of those regulatory genes exhibited distinct or even contrasting expression in leaves and roots in response to Pi starvation, supporting the idea that distinct Pi starvation response strategies are used for different plant organs in response to a shortage of Pi in the growth medium.
Phosphorus is one of the three essential macronutrients of plants. Phosphorus is not only a constituent of such key cell molecules as ATP, nucleic acids, and phospholipids, but it is also a pivotal regulator in many metabolisms, including energy transfer, protein activation, and carbon and amino acid metabolic processes (Marschner, 1995  ). Limitation of phosphate (Pi) causes both molecular and
developmental adaptation in all organisms. In higher plants, Pi limitation
leads to dramatic changes in root growth and architecture, such as an increase
root to shoot ratio, an increase of lateral roots, and an increase of root
hair number and length, thus Pi use can be enhanced
(Bates and Lynch, 1996;
Rubio et al., 2001).
Many molecular adaptation responses have been described from various
organisms. For example, under Pi limitation, both Escherichia coli
and Brewer's yeast (Saccharomyces cerevisiae) activate a
multigene-inducible system to scavenge traces of usable Pi from the
surrounding medium (Torriani,
1990
Pi starvation-responsive genes appear to be involved in multiple metabolic
pathways, implying a complex Pi regulation system in plants. Investigation of
Pi starvation-responsive genes at a genomic level is required to establish a
more complete inventory of the genes and pathways that are responsive to Pi
starvation stress. A whole-genome DNA microarray analysis revealed that the
yeast system consists of more than 20 Pi starvation-regulated genes under the
same control mechanism (Ogawa et al.,
2000
Microarray technology has become a useful tool for the analysis of plant
genome expression profiles under a variety of developmental or environmental
conditions. Recently, several successful studies of gene expression profiles
responsive to environmental cues have been reported. They include light (Ma et
al., 2001
Experimental Design and Plant Pi Concentration Measurements
Wild-type Arabidopsis (Columbia ecotype) seeds were germinated and grown
under normal Pi conditions (Chen et al.,
2000
Two duplicated biological samples for each treatment were used for total
RNA preparation. The ratios of gene expression at each time point after Pi
starvation compared with the control plants were obtained from four to six
replicated hybridizations, including reverse fluorescent dye labeling. The
ratios of both inducible and repressible expression were calculated as
described (Ma et al., 2001
A total of 1,835 genes (about 29% of the total genes on the microarray) exhibited alteration in their RNA expression in response to Pi starvation in at least one of the four time points using a median 2-fold ratio cutoff. The total number of genes that exhibited changes in expression pattern is almost double in leaves (1,398) in comparison with roots (730). There are both overlapping and distinct genes regulated in the leaves and roots. There were totals of 680 and 333 up-regulated genes in leaves and roots, respectively, with 2-fold or higher differential expression for at least one time point. About 192 of those induced genes are shared between leaves and roots, and 488 and 141 are specifically induced in leaves and roots, respectively. There were 718 and 397 genes down-regulated in leaves and roots, respectively. Among them, only 101 genes are shared by roots and leaves, whereas 617 and 296 are specifically repressed in leaves and roots, respectively. Thus the majority of the repressed genes are distinct between roots and leaves upon Pi starvation, suggesting distinct strategies used by those two plant organ types in response to Pi starvation in the growth medium. Across the four time points examined, most of gene expression changes (1,148 and 632 of genes for leaves and roots) showed a similar kinetic pattern, e.g. initiation of induction or repression after 6 h starvation, with maximum induction or repression at 48 h, and a decrease at 72 h (Figs. 2A and 3). Several other kinetic patterns for gene expression changes, however, were also observed. For examples, in leaves, the induction of expression under Pi starvation for 84 and 20 genes peaked at 24 and 72 h, respectively. In roots, 10, 30, and 12 genes were maximally induced at 6, 24, and 72 h, respectively. As for down-regulated genes, 6, 115, and 20 genes were maximally repressed at 6, 24, and 72 h, respectively, in leaves, whereas 7, 9, and 24 genes were maximally repressed at 6, 24, and 72 h, respectively, in root tissue (Fig. 4). As shown in Figure 4, the repression pattern of the genes maximally repressed at 72 h in roots was different from that in leaves. There are also some genes that were induced or repressed at one time point, while oppositely regulated at another time point in the same organ (Fig. 2, B and C).
Those genes whose expression is significantly altered represent a large range of functional categories. On the basis of the recent functional classification of Arabidopsis genes (http://mips.gsf.de/proj/thal/db/search/search_frame.html; http://www.ncbi.nlm.nih.gov), Pi starvation-responsive genes include those involved in cell biogenesis, cellular organization, cellular transport and transport mechanisms, cell division, nucleic acid metabolism, amino acid metabolism, protein synthesis, protein destination, carbon metabolism, photosynthesis, respiration, photo-oxidative respiration, nitrogen, phosphorus and sulfur metabolisms, senescence, transporter facilitation, signal transduction, compartments, transcription, second metabolism, developmental regulation, responses to stresses, and others. Some selected genes involved in carbon and nitrogen assimilation, metabolic adaptations, TFs, and signal transduction are described below. All of the specific genes listed in the figures thereafter and presented below were sequenced to confirm their identity in this study.
Although there was no detectable change of Pi concentration in leaves within 72 h of Pi starvation, representative genes for photosynthesis and nitrogen assimilation were down-regulated after 24 h of Pi starvation, which could lead to a growth arrest. A total of 29 genes involved in photosystem (PS) I, PSII, and Calvin cycle and chlorophyll A/B-binding proteins were repressed 2- to 7-fold after 48 h of Pi starvation in leaves. The expression patterns of the representative genes are shown in Figure 5A. These genes encode components of PSI and PSII, which harvest light energy and coordinately produce ATP through photophosphorylation and NADPH and reduced ferredoxin (Fdx–) catalyzed by Fdx-NADP reductase (FNR) and Fdx-thioredoxin reductase (FTR). There are also genes that encode Rubisco small subunits, glyceraldehyde-3-phosphate dehydrogenase, and sedoheptulose-1,7-bisphosphatase, all key regulatory enzymes in CO2 assimilation, reduction, and the regeneration phase of the Calvin cycle, respectively. The expression of all of those genes were repressed, most of them maximally at 48 h after onset of Pi starvation (Fig. 5A).
The genes for nitrate reductase, nitrite reductase (NiR), Gln synthase (GS), and Glu synthase (Fdx-GOGAT) were repressed by 3- to 5-fold in both leaves and roots after 24 h of starvation (Fig. 5B). The reduction of nitrate to ammonium requires both nitrate reductase and NiR activities. Nitrite reduction requires Fdx as a reductant. In leaf photosynthetic cells, Fdx is reduced in PSI by FTR. In roots, Fdx is reduced in plastids by FNR, which uses NADPH as a reductant. As shown in Figure 5A, FTR and FNR were repressed in both leaves and roots. Thus it is logical that this reduced supply of reductant is correlated with down-regulation of the nitrate assimilation components.
On the other side, the GS/GOGAT cycle is the principle route of the primary
ammonium assimilation and re-assimilation of photorespiratory ammonium and of
the synthesis of Glu and Gln in plants. Two classes of GS isoenzymes are found
in plants, one in chloroplasts and another in the cytosol. Both genes
corresponding to GS were repressed in roots, although marginally or not
affected in leaves. Fdx-GOGAT catalyzes a Fdx-dependent reaction to produce
Glu using Gln and
Interestingly, Glu dehydrogenase (GDH) was induced upon Pi starvation. GDH
can catalyze both the synthesis of Glu using NH4+ and
Together with repression of photosynthetic genes upon Pi starvation, genes
for synthetic pathway components for starch, fatty acids, and lipids were also
repressed. As shown in Figure
5C, those include genes encoding ADP Glc pyrophosphorylase,
There is also a general increase in the expression of genes involved in
cell wall synthesis and degradation. Figure
5C lists several representative genes whose expression is induced
by Pi starvation. For example, the synthesis of non-cellulose cell wall
polysaccharides in the Golgi apparatus uses several nucleotide sugars as
substrates. Beginning with formation of UDP-Glc and GDP-Glc, nucleotide sugar
inter-conversion catalyzed by specific enzymes produces various nucleotide
sugars. UDP-Glc 6-dehydrogenase and uridine diphosphate Glc epimerase are
important enzymes in mediating sugar inter-conversion. The intracellular
During glycolysis, the cellular reductant and ATP can be generated by two alternate pathways. In the first case, NADH is generated in a reaction catalyzed by glyceraldehyde 3-phosphate dehydrogenase, whereas ATP is generated in two reactions catalyzed by 3-phosphoglycerate kinase and pyruvate kinase (PK), respectively. In the second pathway, NADPH is produced through a bypass from glyceraldehyde 3-phosphate directly to 3-phosphoglycerate catalyzed by a non-phosphorylating glyceraldehyde 3-phosphate dehydrogenase (Gap), and ATP is produced by PK. Some genes involved in the second pathway were up-regulated under Pi starvation, whereas those in the first pathway were down-regulated (Fig. 5D). In the cytosol, PEP can be converted to pyruvate in a reaction catalyzed by PK or to malate catalyzed by PEP carboxylase and malate dehydrogenase. Two genes for PEP carboxylase and malate dehydrogenase, respectively, were repressed in both leaves and roots during Pi starvation (Fig. 5D), whereas PK was up-regulated. Thus conversion of PEP to pyruvate, which can be funneled into the citric acid cycle, Ala-related amino acids synthesis, and ethanol and lactate synthesis, becomes the more prominent route during Pi starvation. Consistent with this observation, two genes for Ala glyoxylate aminotransferase, the key enzyme for synthesis of Ala family amino acids, were induced in both leaves and roots upon Pi starvation.
During the 72 h of Pi starvation, plant growth was arrested (Table I). As a metabolic adaptation to the growth arrest, down-regulation of protein synthesis and up-regulation of protein degradation could be expected. Actually, there are 42 ribosomal protein genes whose expression was down-regulated by 2- to 5-fold in leaves, and in most cases in roots as well. Those genes encode both chloroplast and cytosol ribosomal proteins (Fig. 6A). This general repression of protein synthesis machinery correlates well with down-regulation of eIF2, a key cytosol translation initiation factor, in both leaves and roots, especially in roots by more than 12-fold (Fig. 6A). Many cellular proteins contain disulfide bonds critical for their function. The proper formation of disulfide bonds is facilitated by an endoplasmic reticulum-localized enzyme named protein disulfide isomerase. Peptidyl prolyl isomerases catalyze the cis-trans isomerization of X-Pro bonds, which helps the protein reach its final folded confirmation more rapidly. All of these genes involved in protein biosynthesis and assembly were repressed after Pi starvation. It is of interest to note that down-regulation of protein synthesis and assembly (Fig. 6A) came somewhat later than those genes involved in carbon and nitrogen assimilation (Fig. 5, A and B), suggesting that the repression of protein biosynthesis may be triggered by the limitation of carbon and nitrogen resources caused by Pi starvation.
It has been suggested that during nutrient starvation, plants transport a series of cytosolic proteins into the vacuole, where the proteins are degraded into amino acids and carbohydrates that can be exported from senescing tissues. In the vacuole, several proteases such as Cys protease, Asp protease, metalloproteases, and Ser proteases degrade proteins to generate exportable amino acids for cell re-use. All of these protease genes presented in the microarray were induced in leaves and most of them in roots as well (Fig. 6B). It is believed that the protease ClpAP found in chloroplasts plays an important role in the degradation of chloroplast proteins. Two distinct ClpP genes were found to be induced upon Pi starvation. In the ubiquitin-proteasome degradation pathway, proteins destined for degradation are delivered to the proteasome after they are covalently modified by conjugation to a ubiquitin chain. Once ubiquitin tagged, the protein is delivered to the 26S proteasome for degradation. At least 18 genes for ubiquitin and the ubiquitin pathway genes were induced and expression patterns for two of them are present in Figure 6B.
Among the 333 TF genes represented in our microarray, expression for 111 of them (30%) was up- or down-regulated 2-fold or more upon Pi starvation. Among them, 74 were up-regulated, with 14 in both leaves and roots, 52 in leaves only, and eight in roots only. There were 36 TFs whose expression was down-regulated, with four in both leaves and roots, 26 in leaves only, and six in roots only. One gene was induced in roots but repressed in leaves. It is interesting to note that leaves and roots have largely nonoverlapping sets of TFs that are regulated during Pi starvation, implying distinct regulatory changes in leaves and roots. Figure 6A lists those TF genes whose expression is induced or repressed 3-fold or more during Pi starvation.
Among the 111 TFs, eight genes code for MYB proteins. The gene for
MYB-related protein CCA1 was induced more than 6-fold in leaves and more than
3-fold in roots at the 24-h point (Fig.
7A). It is interesting to note that at least two reported TFs that
have been described as eukaryotic regulators of Pi metabolism are MYB family
proteins, including Psr1 from Chlamydomonas reinhardtii
(Wykoff et al., 1999
Among the 435 signaling transduction protein genes in the microarray, the expression of 108 genes (24%) were regulated by 2-fold or more during Pi starvation. Similar to the TFs, there is a largely distinct set of genes that are regulated in leaves and roots. Among those 108 genes, 54 were induced, with 33 in leaves only, 12 in roots only, and nine in both leaves and roots. For the 57 down-regulated genes, 39 were in leaves only, 13 in roots only, and five in both leaves and roots. These genes belong to at least seven distinct classes. Figure 6B lists those genes whose expression is regulated by 3-fold or more, either through induction or repression. It is interesting to note that several induced genes in leaves were already up-regulated at the 24-h point (Fig. 7B), whereas the expression of several genes was already significantly altered at the 6- and 24-h time points. It appears that expression of many signal transduction-related genes responded to Pi starvation signals earlier than the metabolic genes described above.
The signal transduction-related genes belong to essentially all common
groups. There are genes encoding an Rho GTPase of plant (ROP)
mitogen-activated protein kinase (MAPK) cascade components, and
Ca2+- or calmodulin-dependent protein kinase (CDPK) or
CDPK-related protein (CDRK) kinases. One CDPK gene on the microarray was
induced by 16-fold, the largest among signal transduction-related genes. CDPKs
are believed to be involved in the response of plants to environmental
stresses such as low temperatures, drought, pathogen defense response, and
mechanical wounding (Martín and
Busconi, 2001 Three genes for ethylene response were regulated by Pi starvation with three expression patterns: induced in leaves, induced in both leaves and roots, and repressed in leaves but induced in roots. Four genes for auxin response showed two expression patterns: induced and repressed in leaves. The different regulation patterns indicate that Pi starvation could regulate different hormone-dependent signaling pathways in distinct manners.
Pi Starvation-Triggered Cell Rescue System by Reduction of Carbon and Nitrogen Assimilation
Pi starvation responses in most organisms can be divided into two
categories, the specific responses and the general responses
(Wykoff et al., 1998
The general responses cover a variety of metabolic pathways and most of the
26% of the genes in the array exhibited differential expression in response to
Pi starvation. The overall metabolic alteration indicates a Pi
starvation-triggered cell rescue system due to the limitation of C and N
assimilation. It is generally assumed that plants could not maintain normal
metabolisms for more than 1 d under Pi starvation, which is supported by our
data that after 1 d Pi starvation, the Pi concentration in root would be
decreased. It has been reported that under Pi starvation, plants may alter the
rate of the photosynthesis and photosynthetic product partitioning
(Duff et al., 1989 NADPH and reduced Fdx are required in carbon reduction and primary nitrate assimilation. In leaf cells, Pi starvation resulted in reduction of photosynthetic gene expression and photosynthetic activity. Thus Fdx and NADPH levels are declined. This would certainly affect carbon reduction and nitrate assimilation. Thus it is more energy conserving for the cell to reduce the expression of genes for carbon reduction pathways and nitrate assimilation enzymes. In roots, Fdx is reduced by FNR using NADPH as a reductant, which can be provided by reduced carbon imtermediates that are transported to or stored in the roots. A reduction of photosynthetic activity in leaves will most likely affect the NADPH and thus Fdx levels in roots. Therefore, it is expected that genes for Fdx-NiR and Fdx-GOGAT involved in nitrate assimilation would be repressed after 24 h of starvation in both leaves and roots. GDH will be induced by reduction of carbon and organic nitrogen in plants to provide NH4+ for the cycle of Gln to Glu. The gene for GDH was induced in both leaves and roots with more than 4-fold induction in leaves in this case (Fig. 5B).
New sources of energy and nitrogen re-assimilation are required to meet
metabolic and transport demands under Pi starvation. Many genes were
coordinately regulated in the catabolism of proteins and carbon compounds
after 24 h of Pi starvation. The Pi starvation evidently presents a stress to
both roots and leaves. This was not only supported by induced expression of
stress response regulatory genes but was also supported by the strong
induction of stress-inducible genes. For example, the expression of the SEN1
was most strikingly regulated by Pi starvation. It has reported that SEN1 can
be strongly induced in Arabidopsis leaves subjected to senescence by 0.1
mM abscisic acid or 1 mM athephon treatment
(Oh et al., 1996
At least 22 Pi regulated genes have been identified through a whole-genome
DNA microarray analysis in Brewer's yeast
(Ogawa et al., 2000
Negative regulation of Pi starvation has been hypothesized in plants
(Mukatira et al., 2001
Our data revealed that the transition of 30-d-old Arabidopsis plants from normal Pi growth medium to Pi starvation resulted in a more than 20% decrease after 24 h in free available Pi in roots, but it was nearly recovered (to 94% of normal level) by the end of 3rd d. However, no change of free available Pi in leaves was observed during the same period (Table I). The decrease in free available Pi in roots after Pi starvation could potentially serve as the trigger for the alteration in genome expression. However, the maximal 20% reduction in free available Pi in roots would be too small a change to be a sensitive signal for a plant's response to Pi starvation. It is more likely that Arabidopsis roots are able to directly sense the Pi availability of the outside growth medium and are able to relay this perceived information to both roots and leaves for an coordinated response in genome expression.
At least two different signaling mechanisms maintaining Pi homeostasis in
plants have been proposed, one operating at the cellular level and another
involving multiple organs and most probably arising from the shoots
(Raghothama, 1999
Many signals are transduced by protein kinase cascades involving small
GTP-binding proteins and MAPK cascades (MAPKKK/MAPKK/MAPK). Genes for these
proteins involved in the transduction chain were up-regulated in leaves
including MAPKKK and RAC-like GTP-binding protein. Down-regulation of the
genes for calmodulin and MAPKK was also found. One gene for the heterotrimeric
G protein
Up- and down-regulation of genes for ethylene-responsive proteins,
auxin-regulated proteins and gibberellin-responsive proteins were found
(Fig. 7B). It is likely that
ethylene and auxin have roles in altering root architecture and promoting root
hair elongation in response to Pi starvation
(Lynch and Brown, 1997
Uptake studies in the pho2 Arabidopsis mutant, a hyperaccumulator
of Pi in shoots, suggest that the induction of gene expression is initiated in
response to changes in internal concentration of Pi in higher plants
(Dong et al., 1998
Plant Growth Conditions
Arabidopsis ecotype Columbia seeds cold-treated in water at 4°C for 3 d
were planted in vermiculite for seedling development. After 6 d, the seedlings
were transferred to hydroponic growth conditions. Plants were grown in growth
chambers (AR-75L, Percival Scientific, Boone, IA) under the light of a
photosynthetic photon flux density of 150 µmol photons
m–2 s–1 in a
14-h-light/10-h-dark photoperiod. The day/night temperature and humidity were
controlled at 22°C/20°C and 80%. After 30 d, the plants grown
hydroponically in nutrient solution containing 5 mM
KNO3, 2.5 mM KH2PO4, 2
mM MgSO4, 2 mM
Ca(NO3)2, 50 µM Fe-EDTA, 70
µM H3BO4, 14 µM
MnCl2, 0.5 µM CuSO4, 1 µM
ZnSO4, 0.2 µM Na2MoO4, and 0.01
µM CoCl2, pH 5.7 (modified from
Chen et al., 2000
Ten representative plant rosettes and roots were harvested at defined time points after growth medium transition for Pi concentration measurement. After drying in an 80°C oven for 3 d, the Pi concentration of the rosette of each sample was analyzed by the method of phosphomolybdenum blue reaction using a Spectroquant NOVA60 spectrophotometer and Spectro-quant Phosphat-Test Kit (Merck, Darmstadt, Germany). The total free available Pi concentration of each plant was calculated based on the total dried biomass and the Pi content.
Total RNA was extracted from the roots and leaves of Arabidopsis plants by
using Trizol D0410 reagent based on recommended procedure (Invitrogen,
Carlsbad, CA). About 50 to 100 mg of tissue was homogenized using a porcelain
mortar in 1 mL of Trizol reagent, and the isolation procedure was essentially
as previously described (Ma et al.,
2001
All of the EST clones corresponding to specific genes resented in the figures or text have been sequenced to confirmed the identity using a MegaBACE 1000 sequencer. Sequence homologies were examined with the GenBank/EMBL database using the BLAST program.
Probe labeling with Cy-3- or Cy-5-conjugated deoxy UTP (Amersham Pharmacia
Biotech, Piscataway, NJ), the purification of labeled cDNA, hybridization to
the Arabidopsis array, and washing and scanning of hybridized array slides
were as described previously (Ma et al.,
2001
Hybridization signals from the microarray were quantified using Axon
GenePix Pro 3 image analysis software. The expression ratios were measured
using the GenePix Pro 3 median of ratio method, and they were normalized using
the corresponding GenePix default normalization factor. The program GPMERGE
was used to merge the replicated GenePix Pro 3 output data files (gpr files;
http://bioinformatics.med.yale.edu/software.html).
With this program, four to six replicated data sets from each experiment were
pooled. A number of quality control procedures were conducted before data
points from the replicates of two or three independent biological sample sets
were averaged as previously described (Ma et al.,
2001
We thank Jessica Habashi, James Sullivan, Vicente Rubio, and Magnus Holm for reading and commenting on this manuscript. We are grateful to the Yale DNA microarray laboratory of the Keck Biological Resource Center for the production of the microarray used in this study (http://info.med.yale.edu/wmkeck/dna_arrays.htm). Received January 25, 2003; returned for revision March 4, 2003; accepted March 11, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.021022.
1 This work was supported by the National Institutes of Health (grant no.
GM–47850 to X.W.D.), by the National Natural Science Foundation of China
(grant no. 39725002), and by the National Key Basic Research Special
Foundation of China (grant no. G199911700). L.M. is a long-term postdoctoral
fellow of the Human Frontier Science Program.
[w] The online version of this article contains Web-only data. The supplemental
material is available at
http://www.plantphysiol.org. * Corresponding author; e-mail xingwang.deng{at}yale.edu; fax 203–432–3854.
Abel S, Nurnberger T, Ahnert V, Krauss GJ, Glund K (2000) Induction of an extracellular cyclic nucleotide phosphodiesterase as an accessory ribonucleolytic activity during phosphate starvation of cultured tomato cells. Plant Physiol 122: 543–552 Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 21: 529–538 Berben G, Legrain M, Gilliquet V, Hilger F (1990) The yeast regulatory gene PHO4 encodes a helix-loop-helix motif. Yeast 6: 451–454[CrossRef][Web of Science][Medline]
Burleigh SH, Harrison MJ (1999) The
down-regulation of Mt4-like genes by phosphate fertilization occurs
systemically and involves phosphate translocation to the shoots. Plant
Physiol 119:
241–248 Chen DL, Delatorre CA, Bakker A, Abel S (2000) Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 211: 13–22[CrossRef][Web of Science][Medline]
Chico JM, Raíces M, Téllez-Iñón MT,
Ulloa RM (2002) A calcium-dependent protein kinase is
systemically induced upon wounding in tomato plants. Plant
Physiol 128:
256–270 del Pozo JC, Allona I, Rubio V, Leyva A, de la, Pena A, Aragoncillo C, Paz-Ares J (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J 19: 579–589[CrossRef][Web of Science][Medline] Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71: 791–801[CrossRef][Web of Science][Medline] Dong B, Rengel Z, Delhaize E (1998) Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta 205: 251–256[CrossRef][Web of Science][Medline]
Duff SMG, Moorhead GBG, Lefebvre DD, Plaxton WC
(1989) Phosphate starvation inducible: bypasses of adenylate and
phosphate dependent glycolytic enzymes in Brassica nigra suspension
cells. Plant Physiol 90:
1275–1278 Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiol Planta 90: 791–800[CrossRef]
Eisen MB, Spellman PT, Brown PO, Botstein D
(1998) Cluster analysis and display of genome-wide expression
patterns. Proc Natl Acad Sci USA
95:
14863–14868 Goldstein AH, Baertlein DA, Danon A (1989) Phosphate starvation stress an experimental system for molecular analysis. Plant Mol Biol Rep 7: 7–16 Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Physiol Plant Mol Biol 45: 421–445[CrossRef][Web of Science]
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 Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101: 555–567[CrossRef][Web of Science][Medline]
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai
K, Galbraith D, Bohnert H (2001) Gene expression
profiles during the initial phase of salt stress in rice. Plant
Cell 13:
889–905
Lau WW, Schneider KR, O'Shea EK (1998) A
genetic study of signaling processes for repression of PHO5 transcription in
Saccharomyces cerevisiae. Genetics
150:
1349–1359
Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JCA
(2001) A mutant Arabidopsis heterotrimeric g-protein
beta subunit affects leaf, flower, and fruit development. Plant
Cell 13:
2631–2641 Lenburg ME, O'Shea EK (1996) Signaling phosphate starvation. Trends Biochem Sci 21: 383–387[CrossRef][Web of Science][Medline] Liu C, Muchhal US, Raghothama KG (1997) Differential expression of TPSI1, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33: 867–874[CrossRef][Web of Science][Medline] Lynch J, Brown KM (1997) Ethylene and plant responses to nutritional stress. Physiol Plant 100: 613–619[CrossRef]
Ma L, Gao Y, Qu L, Chen Z, Li J, Zhao H, Deng XW
(2002) Genomic evidence for COP1 as repressor of light regulated
gene expression and development in Arabidopsis. Plant
Cell 14:
2383–2398
Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW
(2001) Light control of Arabidopsis development entails
coordinated regulation of genome expression and cellular pathways.
Plant Cell 13:
2589–2607
Ma L, Zhao HY, Deng XW (2003) Analysis of the
mutational effects of the COP/DET/FUS loci on
genome expression profiles reveals their overlapping yet not identical roles
in regulating Arabidopsis seedling development. Development
130:
969–981 Malboobi MA, Hannoufa A, Tremblay L, Lefebvre DD (1998) Towards an understanding of gene regulation during the phosphate starvation response. In JP Lynch, J Deiman, eds, Phosphorous in Plant Biology: Regulatory Roles in Molecular, Cellular, Organismic, and Ecosystem Processes. The American Society of Plant Physiologists, Rockville, MD, pp 215–226 Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403–410[CrossRef][Web of Science][Medline] Marschner A (1995) Mineral Nutrition of Higher Plants. Academic Press, San Diego
Martín ML, Busconi L (2001) A rice
membrane-bound calcium-dependent protein kinase is activated in response to
low temperature. Plant Physiol
125:
1442–1449 Muchhal JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana (ion uptake/yeast complementation). Plant Biol 93: 10519–10523 Muchhal US, Liu C, Raghothama KG (1997) Calcium-ATPase is differentially expressed in phosphate starved roots of tomato. Physiol Planta 101: 540–544[CrossRef]
Muchhal US, Pardo JM, Raghothama KG (1996)
Phosphate transporters from the higher plant Arabidopsis thaliana.
Proc Natl Acad Sci USA 93:
10519–10523
Mukatira UT, Liu C, Varadarajan DK, Raghothama KG
(2001) Negative regulation of phosphate starvation-induced genes.
Plant Physiol 127:
1854–1862
Ogawa N, DeRisi J, Brown PO (2000) New
components of a system for phosphate accumulation and polyphosphate metabolism
in Saccharomyces cerevisiae revealed by genomic expression analysis.
Mol Biol Cell 11:
4309–4321 Oh SA, Lee SY, Chung IK, Lee CH, Nam HG (1996) A senescence associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30: 739–754[CrossRef][Web of Science][Medline] Oshima Y (1997) The phosphatase system in Saccharomyces cerevisiae. Genes Genet Syst 72: 323–334[CrossRef][Web of Science][Medline] Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665–693[CrossRef][Web of Science] Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3: 182–187[Web of Science][Medline] Romeis T, Piedras P, Jonathan DGJ (2001) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response. Plant Cell 12: 803–816
Rubio V, Francisco L, Roberto S, Ana C, Martín JI,
Antonio L, Javier Paz-Ares J (2001) A conserved MYB
transcription factor involved in phosphate starvation signaling both in
vascular plants and in unicellular. Gene Dev
15:
2122–2133
Seki M, Narusaka M, Abe H, Kasuko M, Yamaguchi-Shinozaki K,
Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the
expression pattern of 1,300 Arabidopsis genes under drought and cold stresses
by using a full-length cDNA microarray. Plant Cell
13:
61–72
Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH
(2001) Multiple transcription-factor genes are early targets of
phytochrome A signaling. Proc Natl Acad Sci USA
98:
9437–9442 Theodorou ME, Plaxto WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101: 339–344[Abstract] Torriani A (1990) From cell membrane to nucleotides: the phosphate regulation in Escherichia coli. BioEssays 12: 371–376[CrossRef][Web of Science][Medline] Trull MC, Deikman J (1998) An Arabidopsis mutant missing one acid phosphatase isoform. Planta 206: 544–550[CrossRef][Web of Science][Medline] Wang H, Ma LG, Habashi J, Li JM, Zhao HY, Deng XW (2002) Analysis of far-red light regulated genome expression profiles of phytochrome A pathway mutants in Arabidopsis. Plant J 32: 723–733[CrossRef][Web of Science][Medline]
Wang R, Guegler K, Labrie ST, Crawford NM
(2000) Genomic analysis of a nutrient response in Arabidopsis
reveals diverse expression patterns and novel metabolic and potential
regulatory genes induced by nitrate. Plant Cell
12:
1491–1509 Weigel D (1995) The APETALATA2 domain is related to a novel type of DNA binding domain. Plant Cell 7: 388–389[CrossRef][Web of Science][Medline]
Wykoff DD, Davies JP, Melis A, Grossman AR
(1998) The regulation of photosynthetic electron transport during
nutrient deprivation in Chlamydomonas reinhardtii. Plant
Physiol 117:
129–139
Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K
(1999) Psr1, a nuclear localized protein that regulates
phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci
USA 96:
15336–15341 This article has been cited by other articles:
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ABSTRACT
RESULTS
-glucosidase
(Malboobi et al., 1998
-ketoglutarate as substrates, in coordination with
GS. In the GS/GOGAT cycle, Asp aminotransferase (Asp), which is involved in
producing 
-3 fatty acid desaturase, and 
