JXB Advance Access originally published online on May 23, 2006
Journal of Experimental Botany 2006 57(9):2049-2059; doi:10.1093/jxb/erj158
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
The online version of this article has been published under an Open Access model. Users are entitled to use, reproduce, disseminate, or display the Open Access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and the Society for Experimental Biology are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact: journals.permissions@oxfordjournals.orgThis paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves
1Creative Research Initiative ‘Sousei’ (CRIS), Hokkaido University, N21W10, Kita-ku, Sapporo, 001-0021 Japan
2Graduate School of Agriculture, Hokkaido University, N9W9, Kita-ku, Sapporo, 060-8589 Japan
3National Institute of Agrobiological Sciences, 2-1-2, Kannondai, Tsukuba, Ibaraki, 305-8602 Japan
4Society for Techno-innovation of Agriculture, Forestry and Fisheries, 446-1, Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki, 305-0854 Japan
5Hitachi Software Engineering, 4-12-7, Higashi-Shinagawa, Shinagawa, Tokyo, 140-0002 Japan
*To whom correspondence should be addressed. E-mail: junw{at}chem.agr.hokudai.ac.jp
Received 24 August 2005; Accepted 3 February 2006
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResults and discussionReferences |
|---|
Plants have developed several strategies for coping with phosphorus (P) deficiency. However, the details of the regulation of gene expression of adaptations to low P are still unclear. Using a cDNA microarray, transcriptomic analyses were carried out of the rice genes regulated by P deficiency and P re-supply to P-deficient plants. The OsPI1 gene, which was isolated as the most significant up-regulated gene under –P conditions, was also the most significant down-regulated gene following P re-supply. Many starch metabolism-related genes, as well as several genes for Pi-liberating enzymes, were up-regulated by –P treatment, suggesting a homeostatic contribution to the Pi concentration in leaf tissues. mRNAs for glucanases were also induced by P re-supply: these are suspected to play a role in loosening the cell wall compounds. Most of the genes up-regulated by –P treatment were down-regulated by P re-supply, suggesting that their responses were specific to –P conditions. Conversely, the number of genes up-regulated by P re-supply was also larger following P re-supply than in the –P condition. It is proposed that the genes up-regulated by P re-supply play an important role in P acquisition by P-deficient plants.
Key words: cDNA microarray, phosphorus deficiency, phosphorus re-supply, rice, transcriptome
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Plants have evolved many adaptations to low concentrations of available phosphate in the soil. The induction of high affinity phosphate transporters and the secretion of acid phosphatase and organic acids contribute to the mobilization of phosphate from organic and inorganic substrates and active uptake of phosphorus (P) from the rhizosphere (Gardner et al., 1983; Tadano and Sakai, 1991; Mucchal et al., 1996; Mucchal and Raghothama, 1999; Liu et al., 2001; Kai et al., 2002; Wasaki et al., 2003a). It is also clear that P is efficiently utilized once inside the plant tissue (Duff et al., 1989, 1991). Goldstein et al. (1989) proposed that plants possess a ‘pho regulon’, similar to that observed in yeast (Bergman et al., 1986) and Escherichia coli (Torriani and Ludtke, 1985), which might regulate the expression of genes responsible for adaptations for low P conditions. Many P-deficient inducible genes have been isolated and characterized to clarify the gene regulation system underlying low P adaptation. Transcription elements related to the response to P deficiency have been isolated (Malboobi and Lefebvre, 1997; Rubio et al., 2001); however, not enough is currently known to explain the details of the gene expression-regulating network for low P adaptation.
Recent advances in post-genomic studies have indicated that transcriptomic analysis is a useful tool for understanding gene expression networks. Some transcriptomic studies of low P adaptation strategies have also been carried out using cDNA arrays (Hammond et al., 2003, 2004b; Uhde-Stone et al., 2003; Wu et al., 2003; Wang et al., 2002; Wasaki et al., 2003b; Misson et al., 2005). Wu et al. (2003) and Hammond et al. (2003) reported that the expression of various genes in Arabidopsis, such as the bypass pathways of C metabolism and signal transduction, changes when plants are grown under low P conditions. Wang et al. (2002) developed microarrays containing mineral nutrition-related cDNAs to analyse the transcriptomic changes caused by P, K, and Fe deficiency. Their results suggested that deficiency of these three essential elements caused cross-talk during gene regulation.
The results of transcriptomic analyses on P-deficient rice roots using a cDNA microarray spotted with 8987 redundant expressed sequence tag (EST) clones have been reported previously (Wasaki et al., 2003b). The up-regulation of the genes involved in P uptake and many important metabolic changes in C and N metabolism have been discussed (Wasaki et al., 2003b). Furthermore, the most significant induced gene, designated as OsPI1, has been cloned and characterized (Wasaki et al., 2003c). OsPI1 shares some of the properties of the novel P deficiency-inducible gene family, TPSI1/Mt4. It is thought that the TPSI1/Mt4 family plays an important role in the early stages of adaptation to low P availability because of their early up-regulation after exposure to P-deficient conditions (Liu et al., 1997; Burleigh and Harrison, 1998; Martín et al., 2000; Wasaki et al., 2003c). A split-root experiment revealed that Mt4 gene expression in Medicago truncatula is not regulated by the Pi concentration in roots but by the shoot P status (Burleigh and Harrison, 1999). The pho1 mutant of Arabidopsis, which lacks the ability to load P into the xylem, shows constitutive At4 expression in its shoots even in the presence of an adequate P supply (Martín et al., 2000). These facts together suggest the possibility that the early response-related genes, the TPSI1/Mt4 family, are regulated by shoot P status.
P deficiency causes reduction of leaf expansion and the number of leaves (Marschner, 1995). Carbohydrate metabolism in leaves is also affected by P deficiency (Fredeen et al., 1989). It appears that bypassing glycolysis and the induction of acid phosphatase and RNase enhance internal P recycling and these are thus important adaptations to low P conditions (Duff et al., 1994; Green, 1994; Plaxton, 1996; Nanamori et al., 2004). P in leaves declines partially under P-deficient conditions and is rapidly re-translocated to new leaves (Mimura, 1995; Jeschke et al., 1997). It is apparent, therefore, that although some aspects of plant strategies for coping with P-deficient conditions are understood, the majority are not; a broad view of gene expression is necessary to elucidate fully all of the mechanisms involved. This study used cDNA microarrays to investigate the transcriptomic changes in rice leaves brought about by P deficiency and re-supply.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Plant material
Rice (Oryza sativa L. ssp. japonica cv. Michikogane) plants were germinated and cultured hydroponically under the same conditions described by Wasaki et al. (2003b). +P and –P solutions contained 32 and 0 µM NaH2PO4, respectively. At 8 d after transplanting, half of the plants grown on each of the +P and –P solutions were transferred to –P and +P solutions for short-term –P and P re-supply treatments, respectively. The remaining plants were cultivated in their respective solutions to provide long-term +P and –P treatments. All plants were harvested on the following (i.e. the ninth) day. The fresh weights of the shoots and roots were measured and the plants were then immediately frozen with liquid nitrogen and stored at –80 °C.
Measurement of total P content
The shoots were freeze-dried and ground, then 
50 mg of each sample was digested with H2SO4–H2O2. The P content in the digested solution was measured using the method of Saheki et al. (1985). Briefly, digested solution was mixed with 10 vols of molybdate reagent (15 mM ammonium molybdate, 100 mM zinc acetate, pH 5.0) and 2.5 vols of 10% ascorbic acid. The solution was mixed and incubated for 15 min at 30 °C, and then the absorbance was measured at 850 nm.
RNA extraction and labelling
Total RNAs were extracted by the SDS–phenol method (Palmiter, 1974) and purified by the CsCl gradient ultracentrifuge method (Sambrook et al., 1989). A 40 µg aliquot of purified RNAs was used per array and these were set as the targets for the microarrays. The RNAs were reverse-transcribed and labelled using Superscript II (Gibco BRL, Rockville, MD, USA) with Cy5-dCTP (Amersham Bioscience, Piscataway, NJ, USA). Unlabelled primers and dyes were removed with green fluorescent protein (GFP) columns (Amersham Bioscience).
Microarray analysis
Microarray analysis was performed according to our previously published method (Wasaki et al., 2003b), which briefly is as follows. Rice cDNA microarrays containing 8987 cDNA clones were prepared on two glass slides by the microarray project in Japan (Kishimoto et al., 2002). Hybridization was performed at 60 °C for 4 h. After hybridization, the slides were washed and dried. The signal intensity of each spot was obtained using an array scanner (FLA8000; Fuji Film, Tokyo, Japan) and the scanned signals were analysed using Array Gauge software from Fuji Film. Normalization of the signal intensity gained from each spot was performed using the same method described previously (Wasaki et al., 2003b). Each clone was annotated by the superior known gene identified in a BLAST search, and the significance of the annotation was estimated by whether the e-value was under 1.0e–10.
Investigation of mRNA accumulation using RT–PCR
Isolated RNA was treated with DNase (RT grade, Nippon Gene, Tokyo, Japan) to digest the contaminated genomic DNA, then reverse-transcribed using a 1st Strand cDNA Synthesis Kit for reverse transcription–PCR (RT–PCR) (AMV) (Roche Diagnostics, Basel, Switzerland). The first-strand cDNAs were used as templates for RT–PCR. The RAc1 gene was selected as the control gene because it has been reported that expression of this gene is relatively stable among actin isoforms in rice (McElroy et al., 1990). RT–PCR was performed using Ex Taq (Takara-bio, Shiga, Japan) with three replications. ra1LC-S and ra1LC-A primers, designed previously (Wasaki et al., 2003b), were used for the amplification of RAc1 fragments. The primer sets for the SqdX-like gene, anion channel, ammonia transporter (AMT), Al-inducible EST, and an unknown gene were designed as follows: SqdX-S (sense primer, 5'-CTG GAG TCC ATG TCA TCT GG-3') and SqdX-A (antisense primer, 5'-TCT GTT GAC CTC AGG TGC TG-3'), AC-S (5'-TGC TGT TGG TGC TGA TGT CT-3') and AC-A (5'-TGA ATT ATT GGG GTG CAA GG-3'), AMT1.1-S (5'-AGG ACG AGC ACG ACA AGT CT-3') and AMT1.1-A (5'-CCT GCA CAG CCA CCT ATC TT-3'), wali7-S (5'-CTG GGG GAT AAC TGC TGA TG-3') and wali7-A (5'-CCT GGA GTT CAT TCC TGC TT-3'), and EPI1-S (5'-CAG CAT GGC TTC CAT AGG AT-3') and EPI1-A (5'-CCA TTT CTC TGT TCC TTC CA-3'). To amplify the RAc1 fragments, a thermal cycler (T-gradient, Biometra, Göttingen, Germany) was run at 94 °C for 3 min as the first denaturing step, at 94 °C for 30 s, 65 °C for 30 s, and 72 °C for 30 s for eight cycles for the chain reaction, and then at 72 °C for 30 s as the extension step. To amplify the fragments of the SqdX-like gene, the thermal cycler was run at 94 °C for 2 min as the first denaturing step, at 94 °C for 30 s, 65 °C for 1 min, and 72 °C for 2 min for eight (for the AMT), 10 (for Al-inducible EST and the unknown gene), and 15 cycles (for the SqdX-like gene and anion channel) for the chain reaction, and then at 72 °C for 5 min as the extension step. The PCR products were separated on a 2% agarose gel and blotted on Hybond N+ (Amersham Bioscience). DNA probes were prepared by subcloned PCR fragments. Labelling and hybridization with specific DNA probes were performed using the Gene ImagesTM system (Amersham Bioscience) according to the manufacturer's instructions.
Statistical analysis mh2:
Plant growth and mineral analyses were carried out in triplicate. Significance analyses were performed by Student's t test (P <0.01). Four data set were obtained in microarray analyses; two replications of plant sample and two replications of spots on glass slides.
|
Results and discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
The P concentration in both leaves and roots was markedly lower in the long-term –P treatment (Table 1). In this treatment, the fresh weight of both shoots and roots was also significantly lower (Table 2; the t test was performed at the 1% level). Although the P concentration in both leaves and roots was increased after re-supplying P, the fresh weight of the shoots and roots in the P re-supply treatment was nevertheless lower than that of plants grown with P (Tables 1, 2). The effects of short-term –P treatment on the P concentration and plant growth were negligible (Tables 1, 2).
|
|
The genes up- and down-regulated by the –P treatment are listed in Table 3. There was one up-regulated gene in the short-term (24 h) and 48 genes in the long-term (9 d) –P treatments, whereas there were eight and four down-regulated genes in these two treatments, respectively. The number of genes regulated (especially down-regulated genes) by the P deficiency was lower in leaves than in roots (Wasaki et al., 2003b). It is probable that the responses in gene expression for adaptation to low P conditions are more dynamic in roots than in leaves. There were no genes which were significantly regulated in a similar manner between the short- and long-term –P treatments. This result suggests that the responses in P-deficient rice leaves are different between short- and long-term treatments, whereas those of roots are relatively similar (Wasaki et al., 2003b). Element no. 3526, which was designated OsPI1 (Oryza sativa phosphate-limitation inducible gene 1; Wasaki et al., 2003c), showed the most significant increase in its transcription in the long-term –P treatment, in both the roots and leaves (Table 3a; Wasaki et al., 2003b, c).
|
The genes up- and down-regulated by the P re-supply treatment are listed in Table 4. A greater number of genes were regulated by the P re-supply treatment than by the short- and long-term P deficiency treatments (69 and 32 genes were up- and down-regulated by P re-supply, respectively). Most of the genes down-regulated by P re-supply were up-regulated by long-term –P, suggesting that their responses were specific to the long-term –P condition (Table 4b). Conversely, most of the genes up-regulated by P re-supply were expressed at similar levels in both the +P and long-term –P treatments (Table 4a).
|
Four genes related to P metabolism were induced by long-term –P treatment (Table 3a, ii). Inorganic pyrophosphatase (element no. 3001) and a phosphatase (element no. 6414) probably contributed to the maintenance of the Pi concentration in the tissue by the direct production of Pi from organic phosphate compounds. It was concluded that the function of inorganic pyrophosphatase (element no. 3001) was common in both roots and leaves, because expression was induced in both organs by long-term –P treatment. Both bifunctional nuclease (element no. 8098) and S-like RNase (element no. 8316) expression levels were increased by the –P conditions; their contribution is to produce monomeric nucleotides as substrates for phosphatases (Duff et al., 1994; Green, 1994; Palma et al., 2000), and similar results in rice roots and Arabidopsis have also been reported (Wasaki et al., 2003b, Misson et al., 2005).
It was suggested that the transcription factor PHR1 responsible for P deficiency, isolated by Rubio et al. (2001), played an important role in co-ordinated regulation of many ‘late’ Pi starvation genes, such as RNases, phosphatases, and the TPSI1/Mt4 family, which had PHR1-binding sequences (Franco-Zorrilla et al., 2004, Hammond et al., 2004a). In this study, the confirmative data are shown, i.e. OsPI1, RNase, and phosphatase were up-regulated by long-term –P treatment.
Many genes involved in polysaccharide metabolism were up- and down-regulated by long-term –P and P re-supply treatments, respectively (Tables 3a, 4b, blue). It is probable that the up-regulation of ADP-glucose pyrophosphorylase, which is a key enzyme of starch synthesis, and starch synthetic enzymes such as starch branching enzyme and starch synthases, induces the accumulation of starch in leaves under –P conditions. In fact, there are many reports of the accumulation of starch in the chloroplasts of P-deficient rice and other plants (Fredeen et al., 1989; Usuda and Shimogawara, 1991; Qui and Israel, 1992; Rao et al., 1993; Nomura et al., 1995; Ciereszko et al., 2001). It was suggested that the starch accumulation in leaves grown under P-deficient conditions was caused by the disruption of the export of triose phosphate from the stroma by a decrease in the concentration of P (Nátr, 1992). Nátr (1992) also noticed the liberation of Pi by the enhancement of starch synthesis. Because starch synthesis and the induction of Pi-utilizing enzymes are synchronized, it is a reasonable speculation that the starch accumulation in the P-deficient leaves is a result of the maintenance of the internal Pi concentration.
Many glucanases were up-regulated by P re-supply (Table 4a, blue). In a previous report, modulation of the expression of various genes involved in cell wall metabolism by long-term Pi deficiency was observed (Misson et al., 2005). It was concluded that these glucanases hydrolysed the non-cellulosic cell wall compounds and loosened the cell wall, thus contributing to the process of cell elongation. It has been reported that auxin induces glucanases and the degradation of polysaccharides in the cell wall component (Loescher and Nevins, 1972; Sakurai et al., 1979; Inouhe and Nevins, 1991; Kotake et al., 2000). These reports might be consistent with the up-regulation of some auxin-responding genes (Table 4, iii), implying an increase in auxin function following the re-supply of P. The relationship between auxin and root growth during early P deficiency was indicated, although the role of auxin on the stimulation of root growth under P-deficient conditions is still unclear (Abel et al., 2002). Martín et al. (2000) reported that the induction of P-deficient genes in Arabidopsis is enhanced by external auxin supply during short-term P deficiency (1 day). If auxin production is induced by P re-supply in leaves, it could be beneficial in recovering leaf growth.
The differences in deviation value for all spots between the P re-supply treatment and the +P or long-term –P treatments are plotted in Fig. 3. Most of the genes downregulated by P re-supply were up-regulated by –P, as mentioned. Conversely, the number of genes up-regulated by P re-supply was larger when P was re-supplied than in the long-term –P treatment. This result indicates that the genes up-regulated by P re-supply play an important role in P acquisition in P-deficient plants. Ticconi and Abel (2004) mentioned that Pi replenishment treatment for Pi-deficient plants could provide important insights into understanding the metabolic alteration responsible for Pi availability. A large proportion (38%) of the genes up-regulated by P re-supply were unknown genes: further studies are therefore important to clarify their function in P acquisition.
|
Figure 4 shows a summary of metabolic changes based on the regulation of gene expression in the leaves and roots of rice exposed to –P stress. There is a large difference between leaves and roots in the alteration of gene expression under P-deficient conditions. The major responses in leaves were involved in internal P utilization. In roots, it was indicated that not only internal P utilization but also many genes involved in effective P uptake were up-regulated by long-term P deficiency (Uhde-Stone et al., 2003; Wasaki et al., 2003b). The response in leaves seems to be less dramatic than that in roots analysed with the same cDNA microarrays (Wasaki et al., 2003b); however, it is probable that an important function is regulated in shoots, such as the regulation of the novel TPSI1/Mt4 gene family, which includes rice OsPI1 (Burleigh and Harrison, 1999). Further transcriptomic analyses regarding the as yet unknown genes that are regulated by –P treatments are required, using not partial but all-inclusive cDNA arrays. Also, all the metabolic alterations in P deficiency could not be explained using only transcriptomic data; therefore, further follow-up by biochemical methods is also required to verify the putative metabolic alterations suggested in this study. It is also expected that the proteomic and/or metabolomic approaches with transcriptomic analysis will provide useful information for understanding the P deficiency responses in plants well.
|
|
|
|
Acknowledgements |
|---|
This study was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Rice Genome Project MA-2111).
|
Abbreviations |
|---|
AMT, ammonia transporter; EST, expressed sequence tag; RT–PCR, reverse transcription–PCR; SQDG, sulphoquinovosyl diacylglycerol.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
|---|
Abel S, Ticconi CA, Delatorre CA. (2002) Phosphate sensing in higher plants. Physiologia Plantarum 115:1–8.[CrossRef][Medline]
Bergman LW, McClinton DC, Madden SL, Peris LH. (1986) Molecular analysis of the DNA sequences involved in the transcriptional regulation of the phosphate-repressible acid phosphatase (PHO5) of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 83:6070–6074.
Burleigh SH and Harrison MJ. (1998) Characterization of the Mt4 gene from Medicago truncatula. Gene 216:47–53.[CrossRef][ISI][Medline]
Burleigh SH and Harrison MJ. (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiology 119:241–248.
Ciereszko I, Johansson H, Hurry V, Kleczkowski LA. (2001) Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wild-type and pho mutants of Arabidopsis. Planta 212:598–605.[CrossRef][ISI][Medline]
Duff SMG, Moorhead GBG, Lefevbre DD, Plaxton WC. (1989) Phosphate starvation inducible bypasses of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiology 90:1275–1278.
Duff SMG, Plaxton WC, Lefebvre DD. (1991) Phosphate-starvation response in plant cells: de novo synthesis and degradation of acid phosphatases. Proceedings of the National Academy of Sciences, USA 88:9538–9542.
Duff SMG, Sarath G, Plaxton WC. (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiologia Plantarum 90:1275–1278.
Essigmann B, Güler S, Narang RA, Linke D, Benning C. (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 95:1950–1955.
Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J. (2004) The transcriptional control of plant responses to phosphate limitation. Journal of Experimental Botany 55:285–293.
Fredeen AL, Rao IM, Terry N. (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89:225–230.
Gardner WK, Barber DA, Parbey DG. (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil 70:107–124.[CrossRef][ISI]
Goldstein AH, Baretlein DA, Danon A. (1989) Phosphate starvation stress an experimental system for molecular analysis. Plant Molecular Biology Reporter 7:7–16.
Green PJ. (1994) The ribonucleases of higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 45:421–445.[CrossRef][ISI]
Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ. (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology 132:578–596.
Hammond JP, Broadley MR, White PJ. (2004a) Genetic responses to phosphorus deficiency. Annals of Botany 94:323–332.
Hammond JP, White PJ, Broadley MR. (2004b) Diagnosing phosphorus deficiency in plants. Aspects of Applied Biology 72:89–98.
Inouhe M and Nevins DJ. (1991) Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiology 96:426–431.
Jeschke WD, Kirkby EA, Peuke AD, Pate JS, Hartung W. (1997) Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.). Journal of Experimental Botany 48:75–91.[ISI]
Kai M, Takazumi K, Adachi H, Wasaki J, Shinano T, Osaki M. (2002) Cloning and characterization of four phosphate transporter cDNAs in tobacco. Plant Science 163:837–846.[CrossRef]
Kishimoto N, Yazaki J, Fujii F, Shimbo K, Ohta T, Shimatani Z, Nagata Y, Hashimoto A, Kikuchi S. (2002) Rice cDNA microarray: a powerful tool for transcriptome analysis in rice functional genomics. Recent Research Developments in Plant Biology 2:49–59.
Kotake T, Nakagawa N, Takeda K, Sakurai N. (2000) Auxin-induced elongation growth and expressions of cell wall-bound exo- and endo-ß-glucanases in barley coleoptiles. Plant and Cell Physiology 41:1272–1278.
Liu C, Muchhal US, Raghothama KG. (1997) Differential expression of TPSI1, a phosphate starvation-induced gene in tomato. Plant Molecular Biology 33:867–874.[CrossRef][ISI][Medline]
Liu J, Uhde-Stone C, Li A, Vance C, Allan D. (2001) A phosphate transporter with enhanced expression in proteoid roots of white lupin (Lupinus albus L.). Plant and Soil 237:257–266.[CrossRef][ISI]
Loescher W and Nevins DJ. (1972) Auxin-induced changes in Avena coleoptile cell wall composition. Plant Physiology 50:556–563.
Malboobi MA and Lefebvre DD. (1997) A phosphate-starvation inducible ß-glucosidase gene (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Molecular Biology 34:57–68.[CrossRef][ISI][Medline]
Marschner H. (1995) Mineral nutrition in plants 2nd edn (Academic Press, San Diego).
Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Peña A, Leyva A, Paz-Ares J. (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. The Plant Journal 24:559–567.[CrossRef][ISI][Medline]
McElroy D, Rothenberg M, Reece KS, Wu R. (1990) Characterization of the rice (Oryza sativa) actin gene family. Plant Molecular Biology 15:257–268.[CrossRef][ISI][Medline]
Mimura T. (1995) Homeostasis and transport of inorganic phosphate in plants. Mini review. Plant and Cell Physiology 36:1–7.
Misson J, Raghothama KG, Jain A, et al. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences, USA 102:11934–11939.
Mucchal US, Pardo JM, Raghothama KG. (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 93:10519–10523.
Mucchal US and Raghothama KG. (1999) Transcriptional regulation of plant phosphate transporters. Proceedings of the National Academy of Sciences, USA 96:5868–5872.
Nanamori M, Shinano T, Wasaki J, Yamamura T, Rao IM, Osaki M. (2004) Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice. Plant and Cell Physiology 45:460–469.
Nátr L. (1992) Mineral nutrients—a ubiquitous stress factor for photosynthesis. Photosynthetica 27:271–294.
Nomura M, Imai K, Matsuda T. (1995) Effects of atmospheric partial pressure of carbon dioxide and phosphorus nutrition on the ultrastructure of rice (Oryza sativa L.) chloroplasts. Japanese Journal of Crop Science 64:784–793.
Palma DA, Blumwald E, Plaxton WC. (2000) Upregulation of vacuolar H+-translocating pyrophosphatase by phosphate starvation of Brassica napus (rapeseed) suspension cell cultures. FEBS Letters 486:155–158.[CrossRef][ISI][Medline]
Palmiter RD. (1974) Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of undegraded polysomes and messenger ribonucleic acid. Biochemistry 13:3606–3615.[CrossRef][Medline]
Plaxton WC. (1996) The organization and regulation of plant glycolysis. Annual Review of Plant Physiology and Plant Molecular Biology 47:185–214.[CrossRef][ISI]
Qui J and Israel DW. (1992) Diurnal starch accumulation and utilization in phosphorus-deficient soybean plants. Plant Physiology 98:316–323.
Rao IM, Fredeen AL, Terry N. (1993) Influence of phosphorus limitation on photosynthesis, carbon allocation and partitioning in sugar beet and soybean grown with a short photoperiod. Plant Physiology and Biochemistry 31:223–231.
Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J. (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes and Development 15:2122–2133.
Saheki S, Takeda A, Shimizu T. (1985) Assay of inorganic phosphate in the mild pH range, suitable for measurement of glycogen phosphorylase activity. Analytical Biochemistry 13:3605–3615.
Sambrook J, Fritsch EF, Maniatis T. (1989) Molecular cloning. A laboratory manual 2nd edn (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY).
Sakurai N, Nishitani K, Masuda Y. (1979) Auxin-induced changes in molecular weight of hemicellulosic polysaccharides of Avena coleoptile cell wall. Plant and Cell Physiology 20:1349–1357.
Tadano T and Sakai H. (1991) Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions. Soil Science and Plant Nutrition 37:129–140.
Ticconi CA and Abel S. (2004) Short on phosphate: plant surveillance and countermeasures. Trends in Plant Sciences 9:548–555.
Torriani A and Ludtke DN. (1985) The Pho regulon of Escherichia coli. In Shaechter M, Neidhardt FC, Ingraham J, Kjeldgaard NO (Eds.). The molecular biology of bacterial growth (Jones & Bartlett, Boston) pp. 224–242.
Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL. (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiology 131:1064–1079.
Usuda H and Shimogawara K. (1991) Phosphate deficiency in maize. II. Enzyme activities. Plant and Cell Physiology 32:1313–1317.
Wang Y-H, Gravin DF, Kochian LV. (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiology 130:1361–1370.
Wasaki J, Yamamura T, Shinano T, Osaki M. (2003a) Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant and Soil 248:129–136.[CrossRef]
Wasaki J, Yonetani R, Kuroda S, et al. (2003b) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant, Cell and Environment 26:1515–1523.[CrossRef]
Wasaki J, Yonetani R, Shinano T, Kai M, Osaki M. (2003c) Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytologist 158:239–248.[CrossRef]
Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiology 132:1260–1271.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. Zhou, M. Yamagishi, M. Osaki, and K. Masuda Sugar signalling mediates cluster root formation and phosphorus starvation-induced gene expression in white lupin J. Exp. Bot., July 1, 2008; 59(10): 2749 - 2756. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Calderon-Vazquez, E. Ibarra-Laclette, J. Caballero-Perez, and L. Herrera-Estrella Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels J. Exp. Bot., June 6, 2008; (2008) ern115v2. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Hernandez, M. Ramirez, O. Valdes-Lopez, M. Tesfaye, M. A. Graham, T. Czechowski, A. Schlereth, M. Wandrey, A. Erban, F. Cheung, et al. Phosphorus Stress in Common Bean: Root Transcript and Metabolic Responses Plant Physiology, June 1, 2007; 144(2): 752 - 767. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Yin, F. Shimano, and H. Ashihara Involvement of rapid nucleotide synthesis in recovery from phosphate starvation of Catharanthus roseus cells J. Exp. Bot., March 1, 2007; 58(5): 1025 - 1033. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||