Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation

Plant Journal

Volumn 45, Issue 5, 2006, Pages 712-726

  Shin, Heungsop ^a,c   Shin, Hwa Soo ^a   Chen, Rujin ^a   Harrison, Maria J ^b  

^a PLANT BIOLOGY DIVISION   (United States)

^b Boyce Thompson Institute for Plant Research   (United States)

^c VitroSys Research Institute of Biotechnology   (South Korea)

Author keywords

Mineral nutrition; miRNA; Phosphorus; Roots

Indexed keywords

GENES; GENETIC ENGINEERING; PHOSPHORUS; PLANTS (BOTANY); RNA;

MINERAL NUTRITION; MIRNA; OPEN-READING FRAMES (ORF); PHOSPHATE STARVATION;

PHOSPHATES;

ABSCISIC ACID; BACTERIAL DNA; CYTOKININ; PHOSPHATE; PLANT RNA; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; DNA PROBE; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT; PLANT ROOT; PROMOTER REGION; REPORTER GENE; RNA PROCESSING; SEQUENCE ALIGNMENT;

ABSCISIC ACID; ARABIDOPSIS; CYTOKININS; DNA PROBES; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; PHOSPHATES; PLANT ROOTS; PLANT SHOOTS; PROMOTER REGIONS (GENETICS); RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PLANT; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC;

GENES; GENETIC ENGINEERING; PHOSPHATES; PLANTS; ROOTS;

EID: 33644872219     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02629.x     Document Type: Article

References (80)

1. Abel S. Nurnberger T. Ahnert V. Krauss G.-J. 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
2. Abel S. Ticconi C.A. Delatorre C.A. 2002 Phosphate sensing in higher plants Physiol. Plant. 115 1 8
3. Ames B.N. 1966 Assay of inorganic phosphate, total phosphate and phosphatases Methods Enzymol. 8 115 118
4. Arnon D.I. Hoagland D.R. 1940 Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients Soil Sci. 50 463 483
5. Bahyrycz A. Matsubayashi Y. Ogawa M. Sakagami Y. Konopinska D. 2004 Plant peptide hormone phytosulfokine (PSK-alpha): synthesis of new analogues and their biological evaluation J Peptide Sci. 10 462 469
6. Baldwin J.C. Karthikeyan A.S. Raghothama K.G. 2001 LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato Plant Physiol. 125 728 737
7. Bariola P.A. Howard C.J. Taylor C.B. Verburg M.T. Jaglan V.D. Green P.J. 1994 The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation Plant J. 6 673 685
8. Bartel D.P. 2004 Genomics, biogenesis, mechanism and function Cell 116 281 297
9. Bartel B. Bartel D.P. 2003 MicroRNAs: at the root of plant development? Plant Physiol. 132 709 717
10. Bates T.R. Lynch J.P. 1996 Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability Plant Cell Environ. 19 529 538
11. Bieleski R.L. 1973 Phosphate pools, phosphate transport and phosphate availability Annu. Rev. Plant Physiol. 24 225 252
12. Bozzo G.G. Raghothama K.G. Plaxton W.C. 2002 Purification and characterization of two secreted purple acid phosphatase isozymes from phosphate-starved tomato (Lycopersicon esculentum) cell cultures Eur. J. Biochem. 269 6278 6286
13. Burleigh S.H. Harrison M.J. 1998a Characterization of the Mt4 gene from Medicago truncatula Gene 216 47 53
14. Burleigh S.H. Harrison M.J. 1998b Mt4, a phosphorus starvation-inducible cDNA from Medicago truncatula, which is down-regulated both by phosphorus fertilization and arbuscular-mycorrhizal colonization In Phosphorous in Plant Biology: Regulatory Roles in Molecular Cellular, Organismic, and Ecosystem Processes Lynch J.P. Deikman J. eds Rockville, MD American Society of Plant Physiologists pp 359 360
15. Burleigh S.H. Harrison M.J. 1999 The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots Plant Physiol. 119 241 248
16. Campalans A. Kondorosi A. Crespi M. 2004 Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula Plant Cell 16 1047 1059
17. Carrington J.C. Ambros V. 2003 Role of MicroRNAs in plant and animal development Science 301 336 338
18. Chiou T.J. Liu H. Harrison M.J. 2001 The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface Plant J. 25 1 15
19. Clough S.J. Bent A.F. 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 735 743
20. Daram P. Brunner S. Persson B.L. Amrhein N. Bucher M. 1998 Functional analysis and cell-specific expression of a phosphate transporter from tomato Planta 206 225 233
21. 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
22. Delhaize E. Randall P.J. 1995 Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana Plant Physiol. 107 207 213
23. Dong B. Rengel Z. Delhaize E. 1998 Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana Planta 205 251 256
24. Drew M. 1975 Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley New Phytol. 75 479 490
25. Drew M.C. Saker L.R. 1984 Uptake and long-distance transport of phosphate, potassium and chloride in relation to internal ion concentrations in barley: evidence of non-allosteric regulation Planta 160 500 507
26. Franco-Zorrilla J.M. Martin A.C. 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
27. Goldstein A.H. Baertlein D.A. McDaniel R.G. 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
28. Gustafson A.M. Allen E.A. Givan S. Smith S. Carrington J.C. Kasschau K.D. 2005 ASRP:the Arabidopsis small RNA project database Nucl. Acids Res. 33 D637 D640
29. Guzzo F. Portaluppi P. Grisi R. Barone S. Zampieri S. Franssen H. Levi M. 2005 Reduction of cell size induced by enod40 in Arabidopsis thaliana J. Exp. Bot. 56 507 513
30. Hamburger D. Rezzonico E. Petetot J.M.C. 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
31. Hammond J.P. Bennett M.J. Bowen H.C. Broadley M.R. Eastwood D.C. May S.T. Rahn C. Swarup R. Woolaway K.E. White P.J. 2003 Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants Plant Physiol. 132 578 596
32. Harrison M.J. 1997 The arbuscular mycorrhizal symbiosis: an underground association Trends Plant Sci. 2 54 56
33. Heuwinkel H. Kirkby E.A. Le Bot J. Marschner H. 1992 Phosphorus deficiency enhances molybdenum uptake by tomato plants J. Plant Nutr. 15 549 558
34. Holford I.C.R. 1997 Soil phosphorus: its measurement, and its uptake by plants Aust. J Soil Res. 35 227 239
35. 2O within intact plants of Ricinus communis L J. Exp. Bot. 47 1737 1754
36. Jeschke W.D. Kirkby E.A. Peuke A.D. Pate J.S. Hartung W. 1997 Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.) J. Exp. Bot. 48 75 91
37. Jones-Rhoades M.W. Bartel D.P. 2004 Computational identification of plant microRNAs and their targets, including a stress-induced miRNA Mol. Cell 14 787 799
38. Kelly A.A. Dormann P. 2004 Green light for galactolipid trafficking Curr. Opin. Plant Biol. 7 262 269
39. Lenhard M. Laux T. 2003 Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1 Development 130 3163 3173
40. Liu C. Muchhal U.S. Raghothama K.G. 1997 Differential expression of TPS11, a phosphate starvation-induced gene in tomato Plant Mol. Biol. 33 867 874
41. Liu C. Muchhal U.S. Uthappa M. Kononowicz A.K. Raghothama K.G. 1998a Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus Plant Physiol. 116 91 99
42. Liu H. Trieu A.T. Blaylock L.A. Harrison M.J. 1998b Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi Mol. Plant Microbe Interact. 11 14 22
43. Liu J.Q. Samac D.A. Bucciarelli B. Allan D.L. Vance C.P. 2005 Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport Plant J. 41 257 268
44. Lopez-Bucio J. Hernandez-Abreu E. Sanchez-Calderon L. Nieto-Jacobo M.F. 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
45. Marschner H. 1995 Mineral Nutrition of Higher Plants London London Academic Press
46. Martín A.C. del Pozo J.C. Inglesias 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
47. Matsubayashi Y. Goto T. Sakagami Y. 2004 Chemical nursing: phytosulfokine improves genetic transformation efficiency by promoting the proliferation of surviving cells on selective media Plant Cell Rep. 23 155 158
48. Matthews D.H. Zuker S.M. Turner D.H. 1999 Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure J. Mol. Biol. 288 911 940
49. Mimura T. 1999 Regulation of phosphate transport and homeostasis in plant cells Int. Rev. Cytol. 191 149 200
50. Mimura T. Sakano K. Shimmen T. 1996 Studies on the distribution, re-translocation and homeostasis of inorganic phosphate in barley leaves Plant Cell Environ. 19 311 320
51. Muchhal U.S. Raghothama K.G. 1999 Transcriptional regulation of plant phosphate transporters Proc. Natl Acad. Sci. USA 96 5868 5872
52. Muchhal U.S. Pardo J.M. Raghathama K.G. 1996 Phosphate transporters from the higher plant Arabidopsis thaliana Proc. Natl Acad. Sci. USA 93 101519 110523
53. Mudge S.R. Rae A.L. Diatloff E. Smith F.W. 2002 Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis Plant J. 31 341 353
54. Paszkowski U. Kroken S. Roux C. Briggs S.P. 2002 Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis Proc. Natl Acad. Sci. USA 99 13324 13329
55. Poirier Y. Thoma S. Somerville C. Schiefelbein J. 1991 A mutant of Arabidopsis deficient in xylem loading of phosphate Plant Physiol. 97 1087 1093
56. Raghothama K. 1999 Phosphate acquisition Annu. Rev. Plant Physiol. Mol. Biol. 50 665 693
57. Rausch C. Bucher M. 2002 Molecular mechanisms of phosphate transport in plants Planta 216 23 37
58. Robinson D. 1994 Tansley review no.73: the responses of plants to non-uniform supplies of nutrients New Phytol. 127 635 674
59. Rohrig H. Schmidt J. Miklashevichs E. Schell J. John M. 2002 Soybean ENOD40 encodes two peptides that bind to sucrose synthase Proc. Natl Acad. Sci. USA 99 1915 1920
60. Rohrig H. John M. Schmidt J. 2004 Modification of soybean sucrose synthase by S-thiolation with ENOD40 peptide A Biochem. Biophys. Res. Commun. 325 864 870
61. Rubio V. Linhares F. Solano R. Martin A.C. 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
62. Ryan C.A. Pearce G. Scheer J. Moura D.S. 2002 Polypeptide hormones Plant Cell 14 S251 S264
63. Sakagami Y. 2004 A novel peptide plant cell growth factor, phytosulfokine Nippon Nogeikagaku Kaishi - J. Jpn. Soc. Biosci. Biotechnol. Agrochem. 78 100 105
64. Schachtman D.P. Reid R.J. Ayling S.M. 1998 Phosphorus uptake by plants: from soil to cell Plant Physiol. 116 447 453
65. Sharma V.K. Ramirez J. Fletcher J.C. 2003 The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins Plant Mol. Biol. 51 415 425
66. Shin H. Shin H.S. Dewbre G.R. Harrison M.J. 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. 39 629 642
67. Sunkar R. Zhu J.-K. 2004 Novel and stress-regulated MicroRNAs and other small RNAs from Arabidopsis Plant Cell 16 2001 2019
68. Takechi K. Sakamoto W. Katsuhara M. Murata M. Motoyoshi F. 1999 In situ RNA hybridization using Technovit resin in Arabidopsis thaliana Plant Mol. Biol. Rep. 17 43 51
69. Tang W.H. Kelley D. Ezcurra I. Cotter R. McCormick S. 2004 LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro Plant J. 39 343 353
70. Theodorou M.E. Plaxton W.C. 1993 Metabolic adaptations of plant respiration to nutritional phosphate deprivation Plant Physiol. 101 339 344
71. Ticconi C.A. Abel S. 2004 Short on phosphate:plant surveillance and countermeasures Trends Plant Sci. 9 548 555
72. Ticconi C.A. Delatorre C.A. Lahner B. Salt D.E. Abel S. 2004 Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development Plant J. 37 801 814
73. Vance C. 2001 Symbiotic nitrogen fixation and phosphorus acquisition. plant nutrition in a world of declining renewable resources Plant Physiol. 127 390 397
74. Vance C.P. Uhde-Stone C. Allan D.L. 2003 Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource New Phytol. 157 423 447
75. Versaw W.K. Harrison M.J. 2002 A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses Plant Cell 14 1751 1766
76. 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
77. Wasaki J. Yonetani R. Shinano T. Kai M. Osaki M. 2003 Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status New Phytol. 158 239 248
78. Wen J.Q. Lease K.A. Walker J.C. 2004 DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development Plant J. 37 668 677
79. Williamson L.C. Ribrioux S.P.C.P. Fitter A.H. Ottoline Leyser H.M. 2001 Phosphate availability regulates root system architecture in Arabidopsis Plant Physiol. 126 875 882
80. Wu P. Ma L. Hou X. Wang M. Wu Y. Liu F. Deng X.W. 2003 Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves Plant Physiol. 132 1260 1271