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Planta

, Volume 227, Issue 5, pp 1025–1036 | Cite as

Expression analyses of three members of the AtPHO1 family reveal differential interactions between signaling pathways involved in phosphate deficiency and the responses to auxin, cytokinin, and abscisic acid

  • Cécile Ribot
  • Yong Wang
  • Yves PoirierEmail author
Original Article

Abstract

The PHO1 protein is involved in loading inorganic phosphate (Pi) to the root xylem. Ten genes homologous to AtPHO1 are present in the Arabidopsis thaliana (L.) Heyn genome. From this gene family, transcript levels of only AtPHO1, AtPHO1;H1 and AtPHO1;H10 were increased by Pi-deficiency. While the up-regulation of AtPHO1;H1 and AtPHO1;H10 by Pi deficiency followed the same rapid kinetics and was dependent on the PHR1 transcription factor, phosphite only strongly suppressed the expression of AtPHO1;H1 and had a minor effect on AtPHO1;H10. Addition of sucrose was found to increase transcript levels of both AtPHO1 and AtPHO1;H1 in Pi-sufficient or Pi-deficient plants, but to suppress AtPHO1:H10 under the same conditions. Treatments of plants with auxin or cytokinin had contrasting effect depending on the gene and on the Pi status of the plants. Thus, while both hormones down-regulated expression of AtPHO1 independently of the plant Pi status, auxin and cytokinin up-regulated AtPHO1;H1 and AtPHO1;H10 expression in Pi-sufficient plants and down-regulated expression in Pi-deficient plants. Treatments with abscisic acid inhibited AtPHO1 and AtPHO1;H1 expression in both Pi-sufficient and Pi-deficient plants, but increased AtPHO1;H10 expression under the same conditions. The inhibition of expression by abscisic acid of AtPHO1 and AtPHO1;H1, and of the Pi-starvation responsive genes AtPHT1;1 and AtIPS1, was dependant on the ABI1 type 2C protein phosphatase. These results reveal that various levels of cross talk between the signal transduction pathways to Pi, sucrose and phytohormones are involved in the regulation of expression of the three AtPHO1 homologues.

Keywords

Abscisic acid Arabidopsis Auxin Cytokinin PHO1 Phosphate PHR1 

Abbreviations

2,4-D

2,4-Dichlorophenoxy-acetic acid

ABA

Abscisic acid

ABI1

Abscisic acid insensitive 1

Pi

Inorganic phosphate

PHR1

Phosphate starvation response 1

PHO1

Phosphate deficient 1

Notes

Acknowledgments

This research was funded, in part, from a FNS grant (3100A0-105874) to YP, as well as from the Herbette Foundation and the Etat de Vaud. The authors are grateful to Javier Paz-Ares (Centro Nacional de Biotecnologia, Madrid) for providing seeds of phr1 mutant and Hatem Rouached (University of Lausanne) for critical reading of the manuscript.

References

  1. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, 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 26:1053–1066CrossRefGoogle Scholar
  2. 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 miR399 target gene. Plant Physiol 141:1000–1011PubMedCrossRefGoogle Scholar
  3. Bari RP, Pant BD, Stitt M, Scheible W-R (2006) PHO2, micro RNA399 and PHR1 define a phosphate signalling pathway in plants. Plant Physiol 141:988–999PubMedCrossRefGoogle Scholar
  4. 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 405:191–198PubMedGoogle Scholar
  5. Chiou TJ, 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 18:412–421PubMedCrossRefGoogle Scholar
  6. Ciereszko I, Kleczkowski LA (2002) Effects of phosphate deficiency and sugars on expression of rab18 in Arabidopsis: hexokinase-dependent and okadaic acid-sensitive transduction of the sugar signal. Biochim Biophys Acta 1579:43–49PubMedGoogle Scholar
  7. Cieresko 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 212:598–605CrossRefGoogle Scholar
  8. Ciereszko I, Johansson H, Kleczkowski LA (2005) Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J Plant Physiol 162:343–353PubMedCrossRefGoogle Scholar
  9. Crowe ML, Serizet C, Thareau V, Aubourg S, Rouze P, Hilson P, Beynon J, Weisbeek P, Van Hummelen P, Reymond P, Paz-Ares J, Nietfeld W, Trick M (2003) CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31:156–158PubMedCrossRefGoogle Scholar
  10. Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213PubMedGoogle Scholar
  11. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801PubMedCrossRefGoogle Scholar
  12. Ei-D AMSA, Salama A, Wareing PF (1979) Effects of mineral nutrition on endogenous cytokinins in plants of sunflower (Helianthus annus L.). J Exp Bot 30:971–981CrossRefGoogle Scholar
  13. 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 32:353–360PubMedCrossRefGoogle Scholar
  14. 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 138:847–857PubMedCrossRefGoogle Scholar
  15. Franco-Zorilla 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 39:1033–1037CrossRefGoogle Scholar
  16. 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 14:889–902PubMedCrossRefGoogle Scholar
  17. 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 132:578–586PubMedCrossRefGoogle Scholar
  18. Horgan JM, Wareing PF (1980) Cytokinins and the growth responses of seedlings of Betula pendula Roth. and Acer pseudoplatanus L. to nitrogen and phosphorus deficiency. J Exp Bot 31:525–532CrossRefGoogle Scholar
  19. 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 signalling and hormones. Plant Cell Environ 28:353–364CrossRefGoogle Scholar
  20. Jain M, 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 144:232–247PubMedCrossRefGoogle Scholar
  21. Jeschke WD, Hartung W (2000) Root-shoot interactions in mineral nutrition. Plant Soil 226:57–69CrossRefGoogle Scholar
  22. 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 48:1737–1747CrossRefGoogle Scholar
  23. Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233PubMedCrossRefGoogle Scholar
  24. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2006) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918CrossRefGoogle Scholar
  25. Kobayashi K, Masuda T, Takamiya K-I, Ohta H (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47:238–248PubMedCrossRefGoogle Scholar
  26. Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61:385–393Google Scholar
  27. Koornneef M, Reiuling G, Karssen CM (1984) The isolation and characterization of abscisic acid insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383CrossRefGoogle Scholar
  28. Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556PubMedCrossRefGoogle Scholar
  29. Lejay L, Gansel X, Cerezo M, Tillard P, Mueller 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 15:2218–2232PubMedCrossRefGoogle Scholar
  30. López-Bucio L, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MR, Simpson J, Herrera-Estrella L (2002) Phosphate sensitivity alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256PubMedCrossRefGoogle Scholar
  31. Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey R, 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 in pericycle cell activation. Plant Physiol 137:681–691PubMedCrossRefGoogle Scholar
  32. Martin 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. Plant J 24:559–567PubMedCrossRefGoogle Scholar
  33. Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol Biol 55:727–741PubMedCrossRefGoogle Scholar
  34. 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 102:11934–11939PubMedCrossRefGoogle Scholar
  35. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765PubMedCrossRefGoogle Scholar
  36. Morcuende R, Bari RP, Gibon Y, KZheng W, Datt Pant B, Bläsing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112PubMedCrossRefGoogle Scholar
  37. Müller R, Nilsson L, Krintel C, Nielsen TH (2004) Gene expression during recovery from phosphate starvation in roots and shoots of Arabidopsis thaliana. Physiol Plant 122:233–243CrossRefGoogle Scholar
  38. Müller R, Nilsson L, Nielsen LK, Nielsen TH (2005) Interaction between phosphate starvation signalling and hexokinase-independent sugar sensing in Arabidopsis leaves. Physiol Plant 124:81–90CrossRefGoogle Scholar
  39. Müller R, Morant M, Jarmer H, Nilsson L, Hamborg Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171PubMedCrossRefGoogle Scholar
  40. 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 138:2061–2074PubMedCrossRefGoogle Scholar
  41. Nielsen TH, Krapp A, Roeper-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 21:443–454CrossRefGoogle Scholar
  42. Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, RockvilleGoogle Scholar
  43. Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97:1087–1093PubMedCrossRefGoogle Scholar
  44. Radin JW (1984) Stomatal responses to water stress and abscisic acid in phosphorus deficient cotton plants. Plant Physiol 76:392–394PubMedGoogle Scholar
  45. Raghothama KG (2000) Phosphate transport and signaling. Curr Opin Plant Biol 3:182–187PubMedGoogle Scholar
  46. Rock CD (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396CrossRefGoogle Scholar
  47. Rubio V, Linhares F, Solano R, Martin 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 15:2122–2133PubMedCrossRefGoogle Scholar
  48. Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low-and high-phosphate environments. Plant J 39:629–642PubMedCrossRefGoogle Scholar
  49. Shin H, Shin H-S, Chen R, Harrison MJ (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726PubMedCrossRefGoogle Scholar
  50. 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 50:982–994PubMedCrossRefGoogle Scholar
  51. 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 39:792–796PubMedCrossRefGoogle Scholar
  52. Ticconi CA, Delatorre CA, Abel S (2001) Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol 127:963–972PubMedCrossRefGoogle Scholar
  53. Torrey JG (1976) Root hormones and plant growth. Annu Rev Plant Physiol Plant Mol Biol 27:435–459Google Scholar
  54. Trull MC, Guiltinan MJ, Lynch JP, Deikman J (1997) The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant Cell Environ 20:85–92CrossRefGoogle Scholar
  55. Uhde-Stone C, Zinn KE, Ramirez-Yanez 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 Physiol 131:1064–1079PubMedCrossRefGoogle Scholar
  56. Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG (2002) Phosphite, an analogue of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol 129:1232–1240PubMedCrossRefGoogle Scholar
  57. 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 130:1361–1370PubMedCrossRefGoogle Scholar
  58. 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 135:400–411PubMedCrossRefGoogle Scholar
  59. 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 29:1924–1935PubMedCrossRefGoogle Scholar
  60. Watts S, Rodriguez J, Evans S, Davies W (1981) Roots and shoot growth of plants treated with abscisic acid. Ann Bot 47:595–602Google Scholar
  61. 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 132:1260–1271PubMedCrossRefGoogle Scholar
  62. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138:2087–2096PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Plant Molecular Biology, Biophore BuildingUniversity of LausanneLausanneSwitzerland

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