Abstract
Phosphorus (P) is an essential mineral nutrient required for the plant growth and development. Insufficient P supply triggers extensive physiological and biochemical changes in plants. In this study, we used Affymetrix GeneChip rice genome arrays to analyze the dynamics of rice transcriptome under P starvation. Phosphorus starvation induced or suppressed transcription of 2,317 genes, representing 7.2% of the genes. These changes, mostly transient, affected various cellular metabolic pathways including stress response, primary and secondary metabolism, molecular transport, regulatory process and organismal development. Hundred and thirty (5.6% of 2,317 genes) transcripts were expressed similarly both in root and shoot under P starvation. Comparative analysis between rice and Arabidopsis identified 37 orthologous groups that responded to P starvation demonstrating the existence of conserved P stress coupling mechanism among dicot and monocot plants. Additional analysis of transcription profiles of microRNAs revealed differential expression of miR399 and miR169 under P starvation suggesting their potential roles in plant nutrient homeostasis. Analysis of genome-wide gene expression profiles in P starvation in rice shoot and root, using Affymetrix Rice Genome Chip in this paper, has provided an overview of transcriptional responses to the P starvation condition. This will bring very valuable information and will make a great contribution for investigating the response of rice to P starvation.
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References
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
Alexa A, Rahnenfuhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011
Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci 6:463–470
Barabote RD, Tamang DG, Abeywardena SN, Fallah NS, Fu JYC, Lio JK, Mirhosseini P, Pezeshk R, Podell S, Salampessy ML, Thever MD, Saier MH (2006) Extra domains in secondary transport carriers and channel proteins. Biochim Biophys Acta 1758:1557–1579
Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999
Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 21:529–538
Berglund AC, Sjolund E, Ostlund G, Sonnhammer EL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36:D263–D266
Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8:281–297
Bonnet E, Peer YV, Rouze P (2006) The small RNA world of plants. New Phytol 171:451–468
Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574
Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421
Combier JP, Frugier F, Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2–1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088
Combier JP, Billy F, Gamas P, Biebel A, Rivas S (2008) Trans-regulating of the expression of the transcription factor MtHAP2–1 by a uORF controls root nodule development. Genes Dev 22:1549–1559
Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172
Doerner P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11:1–5
Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975
Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800
Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168
Fang Z, Shao C, Meng Y, Wu P, Chen M (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci 176(2):170–180
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:675–1690
Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043
Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404
Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334
Goldstein AH, Beartlein DA, McDaniel RG (1988) Phosphate starvation inducible metabolism in Lycopersicon esculentum: I. Excretion of acid phosphatase by tomato plants and suspension cultured cells. Plant Physiol 87:711–715
Green PJ (1994) The ribonucleases of higher plants. Annu Rev, Plant Physiol, Plant Mol Biol 45:421–445
Griffiths-Jones S (2006) miRBase: the microRNA sequence database. Methods Mol Biol 342:129–138
Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopericum. Physiol Plantarum 138:226–237
Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386
Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902
Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May TM, 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 Physiol 132:578–596
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
Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Montagu MV, Inze D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101:5146–5151
Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22:2825–2827
Hou XL, Wu P, Jiao FC, Jia QJ, Chen HM, Yu J, Song XW, Yi KK (2005) Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signaling and hormones. Plant, Cell and Environment 28:353–364
Hsieh L-C, Lin S-I, Shih AC-C, Chen J-W, Lin W-Y, Tseng C-Y, Li W-H, Chiou T-J (2009) Uncoveringsmall RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132
Hubner N, Caroline AW, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Müller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ (2005) Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet 37:243–253
Jofuku KD, Boer BG, Montagu MV, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225
Jones-Rhoades MJ, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Jones-Rhoades MJ, Bartel B, Bartel DP (2006) MicroRNAs and their regulatory targets in plants. Annu Rev Plant Biol 57:19–53
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
Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494
Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153
Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139:1597–1611
Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141
Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251
Li L, Liu C, Lian X (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72:423–432
Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, Han B, Zhang Q (2006) Expression profiles of 10, 422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Mol Biol 60:617–631
Lin S-I, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil J-L, Breitler JC, Périn C, Ko S–S, Guiderdoni E, Chiou T-J, Echeverria M (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131
Liu F, Wang Z, Ren H, Shen C, Li Y, Ling H-Q, Wu C, Lian X, Wu P (2010) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62:508–517
Lundmark M, Kner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in esponse to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plantarum 140:57–68
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
Mahalingam R, Gomez-Buitrago AM, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4:R20
Malboobi MA, Lefebvre DD (1997) A phosphate-starvation inducible-glucosidase (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol 34:57–68
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
Mallory A, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet S31-36
Mallory AC, Dugas DV, Bartel DB, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046
Marschner H (1995) Mineral Nutrition of Higher Plants. Academic Press, SanDiego, CA
Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud MC (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939
Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS, Cheung VG (2004) Genetic analysis of genome-wide variation in human gene expression. Nature 430:743–747
Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171
Nakanishi H, Okumura N, Umehara Y, Nishizawa NK, Chino M, Mori S (1993) Expression of a gene specific for iron deficiency (Ids3) in the roots of Hordeum vulgare. Plant Cell Physiol 34:401–410
Nover L, Scharf KD, Gagliardi D, Vergne P, Czarnecka-Verner E, Gurley WB (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones 1:215–223
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182
Olczak M, Morawiecka B, Watorek W (2003) Plant purple acid phosphatases-genes, structures and biological function. Acta Biochim Pol 50:1245–1256
Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–D887
Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible W (2009) Identification of nutrient-responsive Arabidopsis and Rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555
Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts Arabidopsis adaptability to nitrogen limitation. Plant J 50:320–337
Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97:1087–1093
Pozo JC, Allona I, Rubio V, Leyva A, 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 mobilizing/oxidative stress conditions. Plant J 19:579–589
Pré M, Atallah M, Champion A, Vos MD, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357
Raghothama KG (1999) Phosphate acquisition. Ann Rev, Plant Physiol, Plant Mol Biol 50:665–693
Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906
Remm M, Storm CE, Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 314:1041–1052
Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520
Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120
Rubio V, Francisco L, Roberto S, Ana C, Martin 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
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009
Schachtman DP, Shin R (2007) Nutrient Sensing and Signaling: NPKS. Annu Rev Plant Biol 58:47–69
Secco D, Baumann A, Poirier (2010) Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol 152:1693–1704
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
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7, 000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003) An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106:923–930
Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832
Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y (2007) Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J 50:982–994
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Sci 12:301–309
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
Theodoru ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344
Thibaud M-C, Arrighi J-F, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789
Trull MC, Deikman J (1998) An Arabidopsis mutant missing one acid phosphatase isoform. Planta 206:544–550
Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47–62
Uhde-Stone C, Gilbert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248:99–116
Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197
Wang YH, Garvin 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 Physiol 130:1361–1370
Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135:400–411
Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009a) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57:895–904
Wang Z, Hu H, Huang H, Duan K, Wu Z, Wu P (2009b) Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signaling in rice. J Integr Plant Biol 51:663–674
Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Yamagishi M, Osaki M (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523
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 Physiol 132:1260–1271
Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917
Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Bio Chem 282:16369–16378
Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice, 3rd ed. International Rice Research Institute, Manila
Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50:849–859
Zhang Y (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704
Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006a) Conservation and divergence of plant microRNA genes. Plant J 46:243–259
Zhang B, Pan X, Cobb GP, Anderson TA (2006b) Plant microRNA: A small regulatory molecule with big impact. Dev Bio 289:3–16
Zhu T (2003) Global analysis of gene expression using Gene Chip microarrays. Curr Opin Plant Biol 6:1–8
Zhu T, Budworth P, Han B, Brown D, Chang HS, Zou G, Wang X (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8, 300 gene by a high-density oligonucleotide probe array. Plant Physiol Biochem 39:221–242
Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM (2010) MicroRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 178:23–29
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This work was supported by grants from the National Basic Research Program of China (2011CB100304), the National High Technology Research and Development Program of China (2010AA101802) and the National Natural Science Foundation of China (31000932).
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Hongmei Cai and Weibo Xie contributed equally to the paper.
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Supplementary Fig. S1 Number of significantly changed transcripts between treatment (P starvation) and control (normal nutrient) at each time point (1 h, 24 h, 7d) in root and shoot materials detected from the microarray experiment. (A) The number of specific changed and overlapped transcripts between treatment (P starvation) and control (normal nutrient) in root at 1 h (PR1-CR1), 24 h (PR2-CR2) and 7d (PR3-CR3) after P starvation; (B) The number of specific changed and overlapped transcripts between treatment (P starvation) and control (normal nutrient) in shoot at 1 h (PS1-CS1), 24 h (PS2-CS2) and 7d (PS3-CS3) after P starvation; (C) The number of specific changed and overlapped transcripts in root (Root-P) and shoot (Shoot-P) during P starvation. Purple for upregulated genes and green for downregulated genes in A and B.
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Cai, H., Xie, W., Zhu, T. et al. Transcriptome response to phosphorus starvation in rice. Acta Physiol Plant 34, 327–341 (2012). https://doi.org/10.1007/s11738-011-0832-7
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DOI: https://doi.org/10.1007/s11738-011-0832-7