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Phosphorus: Plant Strategies to Cope with its Scarcity

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Cell Biology of Metals and Nutrients

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 17))

Abstract

Low phosphorus (P) availability is considered a major constraint for plant growth and crop productivity; therefore, the ability of plant roots to acquire P from soil and the mechanisms that regulate phosphorous homeostasis in the plant are topics of great interest. Low P availability elicits a Pi-starvation response that includes morphological, metabolic, and physiological changes oriented to increase P availability and the efficiency of P uptake and usage by the plant. Recent advances in the study of the plant responses to low P availability allowed the identification of several key molecular components of the P rescue system. However, the complete signaling pathways, as well as the putative phosphate receptors, remain largely unknown. In this chapter, we review current research aimed at dissecting the components of the biochemical, molecular, and physiological adaptations associated with the plant responses to P starvation and its relation to the efficiency and effectiveness of P uptake and assimilation from rhizosphere.

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References

  • Abel S, Nurnberger T, Ahnert V, Krauss G, 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

    Article  CAS  PubMed  Google Scholar 

  • Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8

    Article  CAS  PubMed  Google Scholar 

  • Abelson PH (1999) A potential phosphate crisis. Science 283:2015–2020

    Article  CAS  PubMed  Google Scholar 

  • Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TG, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26:1053–1066

    Article  CAS  Google Scholar 

  • Amtmann A, Hammond JP, Armengaud P, White PJ (2006) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 43:209–257

    Article  CAS  Google Scholar 

  • Andersson MX, Larsson KE, Tjellstrom H, Liljenberg C, Sandelius AS (2005) The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280:27578–27586

    Article  CAS  PubMed  Google Scholar 

  • Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–132

    Article  CAS  PubMed  Google Scholar 

  • Aung K, Lin S-I, Wu C-C, Huang Y-T, C-l Su, 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 

  • Bar-Yosef O (1991) Root excretions and their environmental effects. Influence on availability of phosphorus. In: Waisel Y, Eshel A (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 529–557

    Google Scholar 

  • Barea JM, Ferrol N, Azcón-Aguilar C, Azcón R (2008) Mycorrhizal symbioses. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Springer, Netherlands, pp 143–163

    Chapter  Google Scholar 

  • Bari R, Pant B, 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 C, Taylor C, Verburg M, Jaglan V, Green P (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685

    Article  CAS  PubMed  Google Scholar 

  • Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250

    Article  CAS  Google Scholar 

  • Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400

    Article  CAS  PubMed  Google Scholar 

  • Benton JJ (1998) Plant nutrition. CRC press, New York

    Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Ann Rev Plant Physiol 24:225–252

    Article  CAS  Google Scholar 

  • Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431

    Article  CAS  Google Scholar 

  • Bould C, Hewitt EJ, Needham P (1986) Diagnosis of mineral disorders in plants, 1st edn. Chemical Publishing, London

    Google Scholar 

  • Bozzo GG, Dunn EL, Plaxton WC (2006) Differential synthesis of phosphate-starvation inducible purple acid phosphatase isozymes in tomato (Lycopersicon esculentum) suspension cells and seedlings. Plant Cell Environ 29:303–313

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247:3–24

    Article  CAS  Google Scholar 

  • Cruz-Ramirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramairez-Chavez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Plant Cell 103:6765–6770

    CAS  Google Scholar 

  • Chen Y, Wang Y, Wu W (2008) Membrane transporters for nitrogen, phosphate and potassium uptake in plants. J Integr Plant Biol 50:835–848

    Article  CAS  PubMed  Google Scholar 

  • Chen Z-H, Nimmo GA, Jenkins GI, Nimmo HG (2007) BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J 405:191–198

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    Article  CAS  PubMed  Google Scholar 

  • Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M (1999) Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 11:2153–2166

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    CAS  PubMed  Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    Article  CAS  PubMed  Google Scholar 

  • Devaiah BN, Nagarajan VK, Raghothama KG (2007b) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145:147–159

    Article  CAS  PubMed  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner H (2005) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108:183–200

    Google Scholar 

  • Doerner P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11:536–540

    Article  CAS  PubMed  Google Scholar 

  • Dolan L (2001) Plant development: the benefits of a change of scene 11:R702–R704

    CAS  Google Scholar 

  • Dörmann P, Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7:112–118

    Article  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 

  • 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. Proc Natl Acad Sci USA 95:1950–1955

    Article  CAS  PubMed  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 

  • Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138:847–857

    Article  CAS  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J 32:353–360

    Article  CAS  PubMed  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Chiou TJ, Lin S, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    Article  CAS  PubMed  Google Scholar 

  • Gahoonia TS, Asmar F, Giese H, Nielsen GG, Nielsen NE (2000) Root released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments. Eur J Agron 12:281–289

    Article  CAS  Google Scholar 

  • Gardner WK, Parbery DG, Barber DA (1982) The acquisition of phosphorus by Lupinus albus L.I. Some characteristics of the soil/root interface. Plant Soil 68:19–32

    Article  CAS  Google Scholar 

  • Gaude N, Nakamura Y, Scheible W, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39

    Article  CAS  PubMed  Google Scholar 

  • Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 85:921–928

    Article  CAS  Google Scholar 

  • Goldstein AH (1992) Phosphate starvation indicuble enzymes and proteins in higher plants. In: Wray JL (ed) Inducible plant proteins their biochemistry and molecular biology. Cambridge University Press, Cambridge, UK, pp 25–44

    Chapter  Google Scholar 

  • Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 97:13979–13984

    Article  CAS  PubMed  Google Scholar 

  • Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177:889–898

    Article  CAS  PubMed  Google Scholar 

  • Hamburger D, Rezzonico E, MacDonald-Comber P, Etétot J, Somerville C, Poirier Y (2002) Identification and characterization of Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902

    Article  CAS  PubMed  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 

  • Hammond JP, Broadley MR, Craigon DJ, Higgins J, Emmerson Z, Townsend H, White PJ, May ST (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1:10

    Article  PubMed  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    Article  CAS  PubMed  Google Scholar 

  • Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97:10649–10654

    Article  PubMed  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Holford ICR (1997) Soil phosphorus: its measurement and its uptake by plants. Aust J Soil Res 35:227–239

    Article  CAS  Google Scholar 

  • Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232–247

    Article  CAS  PubMed  Google Scholar 

  • Jeschke WD, Peuke AD, Pate JS, Hartung W (1997) Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity. J Exp Bot 48:1737–1747

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic-acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257

    Article  CAS  Google Scholar 

  • Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167:863–874

    Article  CAS  PubMed  Google Scholar 

  • Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129

    Article  CAS  Google Scholar 

  • Kai M, Takazumi K, Adachi H, Wasaki J, Shinano T, Osaki M (2002) Cloning and characterization of four phosphate transporter cDNAs in tobacco. Plant Sci 163:837–846

    Article  CAS  Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Jain A, Held AM, Carpita NC, Raghothama KG (2006) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918

    Article  CAS  Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Mukatira UT, Panio DUM, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis transporters. Plant Physiol 130:221–233

    Article  CAS  PubMed  Google Scholar 

  • Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ 21:467–478

    Article  CAS  Google Scholar 

  • Kirk GJ, Santos E, Findenegg GR (1999) Phosphate solubilization by organic anion secretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211:11–18

    Article  CAS  Google Scholar 

  • Kirkby EA, Johnston AE (2008) Soil and fertilizer phosphorus in relation to crop nutrition. In: White PJH (ed) The ecophysiology of plant-phosphorus interactions. Springer, 223, p 177

    Chapter  Google Scholar 

  • Kobayashi K, Awai K, Nakamura M, Nagatani A, Masuda T, Ohta H (2009) Type-B monogalactosyldiacylglycerol synthases are involved in phosphate starvation-induced lipid remodeling, and are crucial for low-phosphate adaptation. Plant J 57:322–331

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Masuda T, Takamiya K, Ohta H (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47:238–248

    Article  CAS  PubMed  Google Scholar 

  • Köck M, Loffler A, Abel S, Glund K (1995) cDNA structure and regulatory properties of a family of starvation-induced ribonucleases from tomato. Plant Mol Biol 27:477–485

    Article  PubMed  Google Scholar 

  • Köck M, Theierl K, Stenzel I, Glund K (1998) Extracellular administration of phosphate sequestering metabolites induces ribonucleases in cultured tomato cells. Planta 204:404–407

    Article  Google Scholar 

  • Lambers HY, Shane MW, Cramer MD, Pearse SJ, Veneklass EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  Google Scholar 

  • Lan M, Comerford NB, Fox TR (1995) Organic anions effect on phosphorus release from spodic horizons. Soil Sci Soc Am J 59:1745–1749

    Article  CAS  Google Scholar 

  • Lejay L, Gansel X, Cerezo M, Tillard P, Muller C, Krapp A, von Wiren N, Daniel-Vedele F, Gojon A (2003) Regulation of root Ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15:2218–2232

    Article  CAS  PubMed  Google Scholar 

  • Lenburg M, O'Shea E (1996) Signaling phosphate starvation. Trends Biochem Sci 21:383–387

    CAS  PubMed  Google Scholar 

  • Li MY, Welti R, Wang XM (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Df1 and Df2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761

    Article  CAS  PubMed  Google Scholar 

  • Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141:674–684

    Article  CAS  PubMed  Google Scholar 

  • Lin S-I, Chiang S-F, Lin W-Y, Chen J-W, Tseng C-Y, Wu P-C, Chiou T-J (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  CAS  PubMed  Google Scholar 

  • Linkohr BI, Williamson LC, Fitter AH, Leyser O (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, de la Vega O, Guevara-Garcia A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453

    Article  PubMed  Google Scholar 

  • Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin pericycle cell activation. Plant Physiol 137:681–691

    Article  PubMed  CAS  Google Scholar 

  • Lynch J, van Beem J (1993) Growth and architecture of seedling roots of common bean genotypes. Crop Sci 33:1253–1257

    Article  Google Scholar 

  • Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467

    Article  CAS  Google Scholar 

  • Manske G, Ortiz-Monasterio J, Van Grinkel M, González R, Rajaram S, Molina E, Vlek P (2000) Traits associated with improved P-uptake efficiency in CIMMYT’s semidwarf spring bread wheat grown on an acid Andisol in Mexico. Plant Soil 221:189–204

    Article  CAS  Google Scholar 

  • Martín AC, del Pozo J, 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. Plant J 24:559–567

    Article  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 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible W (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  CAS  PubMed  Google Scholar 

  • Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353

    Article  CAS  PubMed  Google Scholar 

  • Müller 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

    Article  PubMed  CAS  Google Scholar 

  • Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Vasconcelos MJ, Zhao S, McElver J, Bruce W, Amrhein N (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol 8:186–197

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi H, Okumura N, Umehara Y, Nishizawa N-K, 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

    CAS  PubMed  Google Scholar 

  • Nielsen TH, Krapp A, Röper-Schwarz U, Stitt M (1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant Cell Environ 21:443–454

    Article  CAS  Google Scholar 

  • Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210

    Article  CAS  Google Scholar 

  • Otani T, Ae N, Tanaka H (1996) Uptake mechanisms of crops grown in soils with low P status. II. Significance of organic acids in root exudates of pigeon pea. Soil Sci Plant Nutr 42:553–560

    CAS  Google Scholar 

  • Paciorek T, Friml J (2006) Auxin signaling. J Cell Sci 119:1199–1202

    Article  CAS  PubMed  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Wolf-Rüdiger S (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Torres C, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272

    Article  PubMed  Google Scholar 

  • Pierik R, Sasidharan R, Voesenek L (2007) Growth control by ethylene: adjusting phenotypes to the environment. J Plant Growth Regul 26:188–200

    Article  CAS  Google Scholar 

  • Plaxton WC (2004) Plant response to stress: biochemical adaptations to phosphate deficiency. Encyclopedia of plant and crop science. Taylor & Francis, UK, pp 976–980

    Google Scholar 

  • Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97:1087–1093

    Article  CAS  PubMed  Google Scholar 

  • Poleg YAR, Kang S, Hall JG, Metzenberg RL (1996) NUC-2, a component of the phosphate-regulated signal transduction pathway in Neurospora crassa, is an ankyrin repeat protein. Mol Gen Genet 252:709–716

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    Article  CAS  PubMed  Google Scholar 

  • Rolland F, Sheen J (2005) Sugar sensing and signalling networks in plants. Biochem Soc Trans 33:269–271

    Article  CAS  PubMed  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Javier P-A (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 

  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    Article  CAS  PubMed  Google Scholar 

  • Sadka A, DeWald DB, May GD, Park WD, Mullet JE (1994) Phosphate modulates transcription of soybean VspB and other sugar-inducible genes. Plant Cell 6:737–749

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Gutierrez-Ortega A, Hernandez-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 140:879–889

    Article  CAS  PubMed  Google Scholar 

  • Sanda S, Leustek T, Theisen MJ, Garavito RM, Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276:3941–3946

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084

    Article  CAS  PubMed  Google Scholar 

  • Schunmann PH, Richardson AE, Smith FW, Delhaize E (2004) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot 55:855–865

    Article  CAS  PubMed  Google Scholar 

  • Shin H, Shin H, Chen R, Harrison M (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726

    Article  CAS  PubMed  Google Scholar 

  • Stals H, Inzé D (2001) When plant cells decide to divide. Trends Plant Sci 6:359–364

    Article  CAS  PubMed  Google Scholar 

  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell tpc.107.052068

    Google Scholar 

  • Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796

    Article  CAS  PubMed  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9:548–555

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814

    Article  CAS  PubMed  Google Scholar 

  • Tiessen H (2008) Phosphorus in the global environment. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Springer, Netherlands, pp 1–7

    Chapter  Google Scholar 

  • Ulker B, Somssich IE (2004) WRKY transcription factors: From DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  PubMed  CAS  Google Scholar 

  • Valdés-López O, Hernández G (2008) Transcriptional regulation and signaling in phosphorus starvation: what about legumes? J Integr Plant Biol 10:1213–1222

    Article  CAS  Google Scholar 

  • Vance CP (2008) Plants without arbuscular mycorrhizae. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Springer, Netherlands, pp 117–142

    Chapter  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 

  • Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2;1 influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:1751–1766

    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 

  • 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 

  • Wanner BL (1996) Signal transduction in the control of phosphate-regulated genes of Escherichia coli. Kidney Int 49:964–967

    Article  CAS  PubMed  Google Scholar 

  • White PJ, Broadley MR, Greenwood DJ, Hammond JP (2005) Genetic modifications to improve phosphorus acquisition by roots. In Proceedings 568. International Fertiliser Society, York, UK

    Google Scholar 

  • White PJ, Hammond JP (2008) Phosphorous nutrition of terrestrial plants. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Springer, Netherlands, pp 51–81

    Chapter  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 

  • Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99:5732–5737

    Article  CAS  PubMed  Google Scholar 

  • Zakhleniuk OV, Raines CA, Lloyd JC (2001) pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 212:1432–2048

    Article  Google Scholar 

  • Zhang F, Ma J, Cao YP (1997) Phosphorus deficiency enhances root exudation of low molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raphanus sativus L.) and rape (Brasicca napus L.) plants. Plant Soil 196:261–264

    Article  CAS  Google Scholar 

  • Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Jiao FC, Wu ZC, Li Y, Wang X, He X, Zhong W, Wu P (2008) OsPHR2 Is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146:1673–1686

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct Plant Biol 31:949–958

    Article  CAS  Google Scholar 

  • Zimmermann P, Regierer B, Kossmann J, Frossard E, Amrhein N, Bucher M (2004) Differential synthesis of three purple acid phosphatases from potato. Plant Biol 6:519–528

    Article  CAS  PubMed  Google Scholar 

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Sánchez-Calderón, L., Chacon-López, A., Pérez-Torres, CA., Herrera-Estrella, L. (2010). Phosphorus: Plant Strategies to Cope with its Scarcity. In: Hell, R., Mendel, RR. (eds) Cell Biology of Metals and Nutrients. Plant Cell Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10613-2_8

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