Crossref journal-article
Oxford University Press (OUP)
Plant Physiology (286)
Abstract

AbstractOur aim was to generate and prove the concept of “smart” plants to monitor plant phosphorus (P) status in Arabidopsis. Smart plants can be genetically engineered by transformation with a construct containing the promoter of a gene up-regulated specifically by P starvation in an accessible tissue upstream of a marker gene such as β-glucuronidase (GUS). First, using microarrays, we identified genes whose expression changed more than 2.5-fold in shoots of plants growing hydroponically when P, but not N or K, was withheld from the nutrient solution. The transient changes in gene expression occurring immediately (4 h) after P withdrawal were highly variable, and many nonspecific, shock-induced genes were up-regulated during this period. However, two common putative cis-regulatory elements (a PHO-like element and a TATA box-like element) were present significantly more often in the promoters of genes whose expression increased 4 h after the withdrawal of P compared with their general occurrence in the promoters of all genes represented on the microarray. Surprisingly, the expression of only four genes differed between shoots of P-starved and -replete plants 28 h after P was withdrawn. This lull in differential gene expression preceded the differential expression of a new group of 61 genes 100 h after withdrawing P. A literature survey indicated that the expression of many of these “late” genes responded specifically to P starvation. Shoots had reduced P after 100 h, but growth was unaffected. The expression of SQD1, a gene involved in the synthesis of sulfolipids, responded specifically to P starvation and was increased 100 h after withdrawing P. Leaves of Arabidopsis bearing a SQD1::GUS construct showed increased GUS activity after P withdrawal, which was detectable before P starvation limited growth. Hence, smart plants can monitor plant P status. Transferring this technology to crops would allow precision management of P fertilization, thereby maintaining yields while reducing costs, conserving natural resources, and preventing pollution.

Bibliography

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 Physiology, 132(2), 578–596.

Authors 10
  1. John P. Hammond (first)
  2. Malcolm J. Bennett (additional)
  3. Helen C. Bowen (additional)
  4. Martin R. Broadley (additional)
  5. Dan C. Eastwood (additional)
  6. Sean T. May (additional)
  7. Clive Rahn (additional)
  8. Ranjan Swarup (additional)
  9. Kathryn E. Woolaway (additional)
  10. Philip J. White (additional)
References 102 Referenced 341
  1. Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J Mol Biol  251  :  533–549 (10.1006/jmbi.1995.0454)
  2. Abel S, Ticconi CC, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant  115  :  1–8 (10.1034/j.1399-3054.2002.1150101.x)
  3. Baldwin JC, Karthikeyan AS, Raghothama KG (2001) LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol  125  :  728–737 (10.1104/pp.125.2.728)
  4. Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal  32  :  921–950 (10.1081/CSS-100104098)
  5. 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 (10.1046/j.1365-313X.1994.6050673.x)
  6. Bates TR, Lynch JP (2000) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot  87  :  958–963
  7. Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil  236  :  243–250
  8. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris  316  :  1194–1199
  9. Bieleski RL, Ferguson IB (1983) Physiology and metabolism of phosphate and its compounds. In A Läuchli, RL Bieleski, eds, Encyclopedia of Plant Physiology, New Series, Vol 15A. Springer-Verlag, Berlin, pp 422–449
  10. Bohn HL, McNeal BL, O'Connor GA (1979) Soil Chemistry. John Wiley & Sons, New York
  11. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR,  Görlach J (2001) Growth stage-based analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell  13  :  1499–1510 (10.1105/TPC.010011)
  12. Broadley MR, Burns A, Burns IG (2002) Relationships between phosphorus forms and plant growth. J Plant Nutr  25  :  1075–1088 (10.1081/PLN-120003940)
  13. Broadley MR, Escobar-Gutiérrez AJ, Bowen HC, Willey NJ, White PJ (2001) Influx and accumulation of Cs+ by the akt1 mutant of Arabidopsis thaliana (L.) Heynh. lacking a dominant K+ transport system. J Exp Bot  52  :  839–844
  14. Brinch-Pedersen H, Sørensen LD, Holm PB (2002) Engineering crop plants: getting a handle on phosphate. Trends Plant Sci  7  :  118–125 (10.1016/S1360-1385(01)02222-1)
  15. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science  278  :  1963–1965 (10.1126/science.278.5345.1963)
  16. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T,  Mauch F, Luan S, Zou G, Whitham SA et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell  14  :  559–574 (10.1105/tpc.010410)
  17. Ciereszko 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  :  598–605 (10.1007/s004250000424)
  18. Collins FS, Weissman SM (1984) Directional cloning of DNA fragments at a large distance from an initial probe: a circularization method. Proc Natl Acad Sci USA  81  :  6812–6816
  19. 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 (10.1105/tpc.11.11.2153)
  20. de A Gerhardt LB, Sachetto-Martins G, Contarini MG, Sandroni M, de P  Ferreira R, de Lima VM, Cordeiro MC, de Oliveira DE, Margis-Pinheiro M (1997) Arabidopsis thaliana class IV chitinase is early induced during the interaction with Xanthomonas campestris. FEBS Lett  419  :  69–75 (10.1016/S0014-5793(97)01332-X)
  21. Delhaize E, Randall PJ (1995) Characterisation of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol  107  :  207–213 (10.1104/pp.107.1.207)
  22. del Pozo JC, Allona I, Rubio V, Leyva A, de la Peña 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 mobilising/oxidative stress conditions. Plant J  19  :  579–589 (10.1046/j.1365-313X.1999.00562.x)
  23. Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol  127  :  159–172 (10.1104/pp.127.1.159)
  24. Drew MC (1975) Comparison of the effects of a localised 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 (10.1111/j.1469-8137.1975.tb01409.x)
  25. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant  90  :  791–800 (10.1111/j.1399-3054.1994.tb02539.x)
  26. Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol  109  :  813–820 (10.1104/pp.109.3.813)
  27. 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 (10.1073/pnas.95.4.1950)
  28. Fageria NK, Baligar VC (1999) Phosphorus-use efficiency in wheat geno-types. J Plant Nutr  22  :  331–340
  29. 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  :  1675–1690 (10.1105/tpc.003483)
  30. Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual  29  :  15–23 (10.2134/jeq2000.00472425002900010003x)
  31. 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
  32. Ghassemian M, Waner D, Tchieu J, Gribskov M, Schroeder J (2001) An integrated Arabidopsis annotation database for Affymetrix Genechip data analysis, and tools for regulatory motif searches. Trends Plant Sci  6  :  448–449 (10.1016/S1360-1385(01)02092-1)
  33. Gil P, Liu Y, Orbovic V, Verkamp E, Poff KL, Green PJ (1994) Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol  104  :  777–784 (10.1104/pp.104.2.777)
  34. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol  130  :  1319–1334 (10.1104/pp.011254)
  35. Goldstein AH (1992) Phosphate starvation inducible enzymes and proteins in higher plants. In JL Wray, ed, Society for Experimental Biology Seminar Series 49: Inducible Plant Proteins. Cambridge University Press, Cambridge, UK, pp 25–44 (10.1017/CBO9780511600395.003)
  36. 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 (10.1104/pp.87.3.716)
  37. Gonzàlez-Meler MA, Giles L, Thomas RB, Siedow JN (2001) Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply. Plant Cell Environ  24  :  205–215 (10.1111/j.1365-3040.2001.00674.x)
  38. Greenwood DJ, Karpinets TV, Stone DA (2001) Dynamic model for the effects of soil P and fertilizer P on crop growth, P uptake and soil P in arable cropping: model description. Ann Bot  88  :  279–291 (10.1006/anbo.2001.1458)
  39. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C,  Poirier Y (2002) Identification and characterisation of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell  14  :  889–902 (10.1105/tpc.000745)
  40. Haran S, Logendra S, Seskar M, Bratanova M, Raskin I (2000) Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol  124  :  615–626 (10.1104/pp.124.2.615)
  41. Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol  50  :  219–243 (10.1146/annurev.arplant.50.1.361)
  42. Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res  35  :  227–239 (10.1071/S96047)
  43. Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci  164  :  121–129 (10.1002/1522-2624(200104)164:2<121::AID-JPLN121>3.0.CO;2-6)
  44. Kai M, Takazumi K, Adachi H, Wasaki J, Shinano T, Osaki M (2002) Cloning and characterisation of four phosphate transporter cDNAs in tobacco. Plant Sci  163  :  837–846 (10.1016/S0168-9452(02)00233-9)
  45. Karthikeyan AS, Varadarajan DK, Mukatira UT, Panio D'Urzo M, Damsz  B, Raghothama KG (2002) Regulated expression of Arabidopsis transporters. Plant Physiol  130  :  221–233 (10.1104/pp.020007)
  46. 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 (10.1105/tpc.004747)
  47. 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 (10.1104/pp.008532)
  48. Lansford R, Bearman G, Fraser SE (2001) Resolution of multiple green fluorescent protein color variants and dyes using two-photon microscopy and imaging spectroscopy. J Biomed Optics  6  :  311–318 (10.1117/1.1383780)
  49. Li D, Zhu H, Liu K, Liu X, Leggewie G, Udvardi M, Wang D (2002) Purple acid phosphatases of Arabidopsis thaliana. J Biol Chem  2  77:  27772–27781 (10.1074/jbc.M204183200)
  50. Lipton DS, Blancher RW, Blevins DG (1987) Citrate, malate and succinate concentrations in exudates from P-sufficient and P-starved Medicago sativa L. seedlings. Plant Physiol  85  :  315–317 (10.1104/pp.85.2.315)
  51. López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci  160  :  1–13 (10.1016/S0168-9452(00)00347-2)
  52. Lynch PJ (1995) Root architecture and plant productivity. Plant Physiol  109  :  7–13 (10.1104/pp.109.1.7)
  53. Mackerness SAH, John CF, Jordan B, Thomas B (2001) Early signalling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett  489  :  237–242 (10.1016/S0014-5793(01)02103-2)
  54. 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 (10.1186/gb-2003-4-3-r20)
  55. Malboobi MA, Lefebvre DD (1997) A phosphate-starvation inducible β-glucosidase (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol Biol  34  :  57–68
  56. Martín 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  :  559–567 (10.1046/j.1365-313x.2000.00893.x)
  57. Menges M, Hennig L, Gruissem W, Murray JAH (2002) Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem  277  :  41987–42002 (10.1074/jbc.M207570200)
  58. Miller SS, Liu J, Allan DL, Menzhuber CJ, Fedorova M, Vance CP (2001) Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiol  127  :  594–606 (10.1104/pp.010097)
  59. Moseyko N, Zhu T, Chang HS, Wang X, Feldman LJ (2002) Transcriptional profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol  130  :  720–728 (10.1104/pp.009688)
  60. Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA  93  :  10519–10523 (10.1073/pnas.93.19.10519)
  61. Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of Pht1 family of phosphate transporters in Arabidopsis. Plant J  31  :  341–353 (10.1046/j.1365-313X.2002.01356.x)
  62. Mukatira UT, Liu C, Varadarajan DK, Raghothama KG (2001) Negative regulation of phosphate starvation-inducible genes. Plant Physiol  127  :  1854–1862 (10.1104/pp.010876)
  63. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant  15  :  473–497 (10.1111/j.1399-3054.1962.tb08052.x)
  64. National Research Council (1989) Alternative Agriculture. National Academic Press, Washington, DC
  65. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J  33  :  633–650 (10.1046/j.1365-313X.2003.01657.x)
  66. 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 (10.1379/1466-1268(1996)001<0215:THWCAP>2.3.CO;2)
  67. Plaxton WC, Carswell MC (1999) Metabolic aspects of phosphate starvation in plants. In HR Lerner, ed, Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganisation. Marcel Dekker, New York, pp 349–372
  68. Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol  97  :  1087–1093 (10.1104/pp.97.3.1087)
  69. Potter S, Uknes S, Lawton K, Winter AM, Chandler D, DiMaio J, Novitzky  R, Ward E, Ryals J (1993) Regulation of a hevein-like gene in Arabidopsis. Mol Plant-Microbe Interact  6  :  680–685 (10.1094/MPMI-6-680)
  70. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol  50  :  665–693 (10.1146/annurev.arplant.50.1.665)
  71. Ramonell KM, Zhang B, Ewing RM, Chen Y, Xu D, Stacey G, Somerville  S (2002) Microarray analysis of chitin elicitation in Arabidopsis thaliana. Mol Plant Pathol  3  :  301–311 (10.1046/j.1364-3703.2002.00123.x)
  72. Reuber TL, Ausubel FM (1996) Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell  8  :  241–249
  73. 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 (10.1105/tpc.12.5.707)
  74. Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminium induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol  116  :  409–418 (10.1104/pp.116.1.409)
  75. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol  127  :  635–674 (10.1111/j.1469-8137.1994.tb02969.x)
  76. Rouse DT, Marotta R, Parish RW (1996) Promoter and expression studies on an Arabidopsis thaliana dehydrin gene. FEBS Lett  381  :  252–256 (10.1016/0014-5793(96)00051-8)
  77. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol  130  :  1109–1120 (10.1104/pp.005595)
  78. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares  J (2001) A conserved MYB transcription factor in phosphate starvation signalling both in vascular plants and in unicellular algae. Gene Dev  15  :  2122–2133 (10.1101/gad.204401)
  79. Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global security. In H Tiessen, ed, Phosphorus in the Global Environment: Transfers, Cycles and Management. John Wiley & Sons, New York, pp 27–42
  80. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol  116  :  447–453 (10.1104/pp.116.2.447)
  81. Sharma YK, Davis KR (1994) Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol  105  :  1089–1096
  82. Sharpley A (1995) Identifying sites vulnerable to phosphorus loss in agricultural runoff. J Environ Qual  24  :  947–951 (10.2134/jeq1995.00472425002400050024x)
  83. Smethurst PJ (2000) Soil solution and other soil analyses as indicators of nutrient supply: a review. Forest Ecol Man  138  :  397–411 (10.1016/S0378-1127(00)00426-6)
  84. Somssich IE, Wernert P, Kiedrowski S, Hahlbrock K (1996) Arabidopsis thaliana defence-related protein ELI3 is an aromatic alcohol:NADP+ oxidoreductase. Proc Natl Acad Sci USA  93  :  14199–14203 (10.1073/pnas.93.24.14199)
  85. Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE,  Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J  14  :  365–370 (10.1046/j.1365-313X.1998.00136.x)
  86. Trull MC, Deikman J (1998) An Arabidopsis mutant missing one acid phosphatase isoform. Planta  206  :  544–550
  87. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S,  Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell  4  :  645–656
  88. Ullrich-Eberius CI, Novacky A, van Bel AJE (1984) Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta  161  :  46–52 (10.1007/BF00951459)
  89. Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol  127  :  390–397
  90. Vatamaniuk OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci USA  96  :  7110–7115 (10.1073/pnas.96.12.7110)
  91. 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
  92. Visser NV, Hink MA, Borst JW, van der Krogt GNM, Visser AJWG (2002) Circular dichroism spectroscopy of fluorescent proteins. FEBS Lett  521  :  31–35 (10.1016/S0014-5793(02)02808-9)
  93. Wang WC, Liu ZH (1999) HarpinPSS-induced peroxidase and lignin accumulation in tobacco during the hypersensitive response. Aust J Plant Physiol  26  :  265–272
  94. 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 (10.1104/pp.008854)
  95. Wei-jun S, Forde BG (1989) Efficient transformation of Agrobacterium ssp. by high voltage electroporation. Nucleic Acids Res  17  :  8385
  96. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol  126  :  875–882 (10.1104/pp.126.2.875)
  97. Winge P, Brembu T, Bones AM (1997) Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol Biol  35  :  483–495 (10.1023/A:1005804508902)
  98. Withers PJA, Edwards AC, Foy RH (2001) Phosphorus cycling in UK agriculture and implications for phosphorus loss from soil. Soil Use Manag  17  :  139–149 (10.1079/SUM200181)
  99. Xu W, Campbell P, Vargheese AK, Braam J (1996) The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression. Plant J  9  :  879–889 (10.1046/j.1365-313X.1996.9060879.x)
  100. 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 (10.1073/pnas.082696499)
  101. Zakhleniuk OV, Raines CA, Lloyd JC (2001) pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta  212  :  529–534 (10.1007/s004250000450)
  102. 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 8300 gene by a high-density oligonucleotide probe array. Plant Physiol Biochem  39  :  221–242 (10.1016/S0981-9428(00)01234-1)
Dates
Type When
Created 22 years, 2 months ago (June 11, 2003, 11:27 p.m.)
Deposited 8 months, 1 week ago (Dec. 12, 2024, 3:47 p.m.)
Indexed 2 weeks, 5 days ago (Aug. 7, 2025, 4:52 a.m.)
Issued 22 years, 2 months ago (June 1, 2003)
Published 22 years, 2 months ago (June 1, 2003)
Published Online 22 years, 2 months ago (June 1, 2003)
Published Print 22 years, 2 months ago (June 1, 2003)
Funders 0

None

@article{Hammond_2003, title={Changes in Gene Expression in Arabidopsis Shoots during Phosphate Starvation and the Potential for Developing Smart Plants}, volume={132}, ISSN={0032-0889}, url={http://dx.doi.org/10.1104/pp.103.020941}, DOI={10.1104/pp.103.020941}, number={2}, journal={Plant Physiology}, publisher={Oxford University Press (OUP)}, author={Hammond, John P. and Bennett, Malcolm J. and Bowen, Helen C. and Broadley, Martin R. and Eastwood, Dan C. and May, Sean T. and Rahn, Clive and Swarup, Ranjan and Woolaway, Kathryn E. and White, Philip J.}, year={2003}, month=jun, pages={578–596} }