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Gene expression profiles in rice roots under low phosphorus stress

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Abstract

Phosphorus (P), an important plant macronutrient, is a component of key molecules such as nucleic acids, phospholipids and ATP. P is often the limiting nutrient for crop yield potential because of the low concentration of soluble P that can be absorbed directly by plant. Plants have evolved a series of molecular and morphological adaptations to cope with P limitation. However, the molecular bases of these responses to P deficiency have not been thoroughly elucidated. In this report, the gene expression profiles of low-P-tolerant rice Zhongzao 18 (Oryza sativa ssp. Indica) and not-low-P-tolerant rice Lagrue (Oryza sativa ssp. Indica) roots at 6 h, 24 h and 72 h under low P stress were investigated and compared with a control (normal P conditions) profile, using a DNA chip of 60,000 oligos (70 mer) that represented all putative genes of the rice genome. A total of 1,518 and 2,358 genes exhibited alterations in expression in response to low P stress in at least one of the three time points in rice Zhongzao 18 and rice Lagrue, respectively. The differentially expressed genes included those involved in phosphate (Pi) transportation, transportations except for Pi transportation, phosphatase, enzymes other than phosphatase, primary metabolism, secondary metabolism and so on. Several genes involved in glycolysis and TCA cycle were up-regulated during the early stages of low P treatment in rice Zhongzao 18 roots, but not in rice Lagrue roots. The results may provide useful information to further studies of the molecular mechanism of plant adaptation to low P and thus facilitate research in improving P utilization in crop species.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Aung K, Lin S-I, Wu C-C, Huang Y-T, Su C-l, Chiou T-J (2006) Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  CAS  PubMed  Google Scholar 

  • Baldwin JC, Karthikeyan AS, Raghothama KG (2001) LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125:728–737

    Article  CAS  PubMed  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible W-R (2006) PHO2, MicroRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  PubMed  Google Scholar 

  • Bariola PA, Howard CJ, Taylor CP, 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

    Article  CAS  PubMed  Google Scholar 

  • Chiou T-j, Aung K, Lin S-I, Wu C-C, Chiang S-F, Su C-l (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Clarke AE, Newbigin E (1996) Molecular characterization of an S-like RNase of Nicotiana alata that is induced by phosphate starvation. Plant Mol Biol 31:227–238

    Article  CAS  PubMed  Google Scholar 

  • Drew MC, He C-j, Morgan PW (1989) Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiol 91:266–271

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Duff SMG, Moorhead GBG, Lefebvre DD (1989) Phosphate starvation inducible ‘Bypasses’ of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiol 90:1275–1278

    Article  CAS  PubMed  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiol Planta 90(4):791–800

    Article  CAS  Google Scholar 

  • Franco-Zorrilla JM, Gonzalez E, Bustos R, Linhares F, Leyva A, Paz-Ares J (2004) The transcriptional control of plant responses to phosphate limitation. J Exp Bot 55:285–293

    Article  CAS  PubMed  Google Scholar 

  • Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7:270–276

    Article  CAS  PubMed  Google Scholar 

  • Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Physiol Plant Mol Biol 45:421–445

    Article  CAS  Google Scholar 

  • Grierson PF (1992) Organic acids in the rhizosphere of Banksia integrifolia L.F. Plant Soil 144(2):259–265

    Article  CAS  Google Scholar 

  • 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 Physiol 132:578–596

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lipton DS, Blancher RW, Blevins DG (1987) Citrate, malate and succinate concentrations in exuduates from P-sufficient and P-starved Medicago sativa L. seedlings. Plant Physiol 85:315–317

    Article  CAS  PubMed  Google Scholar 

  • Ma L, Chen C, Liu X, Jiao Y, Su N, Li L, Wang X, Cao M, Sun N, Zhang X, Bao J, Li J, Pedersen S, Bolund L, Zhao H, Yuan L, Wong GK-S, Wang J, Deng XW, Wang J (2005) A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. Genome Res 15:1274–1283

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mir G, Domenech J, Huguet G, Guo WJ, Goldsbrough P, Atrian S, Molinas M (2004) A plant type 2 metallothionein(MT) from cork tissue responds to oxidative stress. J Exp Bot 55:2483–2493

    Article  CAS  PubMed  Google Scholar 

  • 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 M-C (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

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun D-J, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  CAS  PubMed  Google Scholar 

  • Muchhal US, Raghothama KG (1999) Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci USA 96:5868–5872

    Article  CAS  PubMed  Google Scholar 

  • Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K-i, Ohta H (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280:7469–7476

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214

    Article  CAS  PubMed  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  CAS  PubMed  Google Scholar 

  • Roosens N, Bernard C, Leplae R, Verbruggen N (2004) Evidence for copper homeostasis function metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett 577(1):9–16

    Article  CAS  PubMed  Google Scholar 

  • 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 Dev 15:2122–2133

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plant: from soil to cell. Plant Physiol 116:447–453

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuko M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinosaki 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

    Article  CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26 s proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  PubMed  Google Scholar 

  • Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3

    Google Scholar 

  • Toyota K, Koizumi N, Sato F (2003) Transcriptional activation of phosphoenolpyruvate carboxylase by phosphorus deficiency in tobacco. J Exp Bot 54:961–969

    Article  CAS  PubMed  Google Scholar 

  • Ueki K (1978) Control of phosphatase release from cultured tobacco cells. Plant Cell Physiol 19(3):385–392

    CAS  Google Scholar 

  • 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 phosphorous deficiency. Plant Physiol 131:1064–1079

    Article  CAS  PubMed  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P (2006) Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ 29:1924–1935

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57:895–904

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30(4):e15

    Article  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cook JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Manila, pp 61–67

    Google Scholar 

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Acknowledgments

This work was supported by the National Special Key Project of Functional Genomics and Biochips (Grant No. 2002AA2Z1002). We thank Prof. Qifa Zhang for the comments and suggestions, and Prof. Liyuan He for providing the seeds of rice Zhongzao 18 and rice Lagrue.

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Correspondence to Lihua Li.

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Li, L., Liu, C. & Lian, X. Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72, 423–432 (2010). https://doi.org/10.1007/s11103-009-9580-0

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  • DOI: https://doi.org/10.1007/s11103-009-9580-0

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