Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation

Plant Cell and Environment

Volumn 38, Issue 1, 2015, Pages 172-187

  Pant, Bikram Datt ^a   Pant, Pooja ^a   Erban, Alexander ^b   Huhman, David ^a   Kopka, Joachim ^b   Scheible, Wolf Rüdiger ^a  

^a PLANT BIOLOGY DIVISION   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Metabolite profiling; MicroRNA; pho2; Phosphate; phr1 mutant; Roots; Shoots

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

3-PHOSPHOGLYCERATE; ARABIDOPSIS PROTEIN; GLYCERIC ACID; MICRORNA; MIRN399 MICRORNA, ARABIDOPSIS; PHO2 PROTEIN, ARABIDOPSIS; PHOSPHORUS; PHR1 PROTEIN, ARABIDOPSIS; PLANT RNA; TRANSCRIPTION FACTOR; UBIQUITIN CONJUGATING ENZYME;

ARABIDOPSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METABOLOME; MUTATION; PHENOTYPE; PLANT; PLANT ROOT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GLYCERIC ACIDS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MICRORNAS; MUTATION; PHENOTYPE; PHOSPHORUS; PLANT ROOTS; PLANT SHOOTS; RNA, PLANT; TRANSCRIPTION FACTORS; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84929314503     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12378     Document Type: Article

References (107)

1. Allwood J.W., Erban A., de Koning S., Dunn W.B., Luedemann A., Lommen A., Goodacre R. (2009) Inter-laboratory reproducibility of fast gas chromatography-electron impact-time of flight mass spectrometry (GC-EI-TOF/MS) based plant metabolomics. Metabolomics: Official Journal of the Metabolomic Society 5, 479-496.
2. Araújo W.L., Ishizaki K., Nunes-Nesi A., Larson T.R., Tohge T., Krahnert I., ... Fernie A.R. (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. The Plant Cell 22, 1549-1563.
3. Aung K., Lin S.I., Wu C.C., Huang Y.T., Su C.L. & Chiou T.J. (2006) Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141, 1000-1011.
4. Badri D.V. & Vivanco J.M. (2009) Regulation and function of root exudates. Plant, Cell and Environment 32, 666-681.
5. Bari R., Pant B.D., Stitt M. & Scheible W.-R. (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988-999.
6. 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. The Plant Journal: For Cell and Molecular Biology 6, 673-685.
7. Bariola P.A., MacIntosh G.C. & Green P.J. (1999) Regulation of S-like ribonuclease levels in Arabidopsis. Antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiology 119, 331-342.
8. Bates R. & Lynch J.P. (2001) Root hairs confer a competitive advantage under low phosphate availability. Plant and Soil 236, 243-250.
9. Borevitz J.O., Xia Y., Blount J., Dixon R.A. & Lamb C. (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. The Plant Cell 12, 2383-2394.
10. Bulgarelli D., Schlaeppi K., Spaepen S., Ver Loren van Themaat E. & Schulze-Lefert P. (2013) Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology 64, 807-838.
11. Bustos R., Castrillo G., Linhares F., Puga M.I., Rubio V., Perez-Perez J., ... Paz-Ares J. (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics 6, e1001102.
12. Cairns A.J. (2003) Fructan biosynthesis in transgenic plants. Journal of Experimental Botany 54, 549-567.
13. Chae L., Lee I., Shin J. & Rhee S.Y. (2012) Towards understanding how molecular networks evolve in plants. Current Opinion in Plant Biology 15, 177-184.
14. Chaparro J.M., Badri D.V., Bakker M.G., Sugiyama A., Manter D.K. & Vivanco J.M. (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS ONE 8, e55731.
15. Chiou T.J., Aung K., Lin S.I., Wu C.C., Chiang S.F. & Su C.L. (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. The Plant Cell 18, 412-421.
16. Cordell D., Drangert J.-O. & White S. (2009) The story of phosphorus: Global food security and food for thought. Global Environmental Change 19, 292-305.
17. Czechowski T., Stitt M., Altmann T., Udvardi M.K. & Scheible W.R. (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5-17.
18. Dakora F.D. & Phillips D.A. (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35-47.
19. Dean J.V., Mohammed L.A. & Fitzpatrick T. (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221, 287-296.
20. Delhaize E. & Randall P.J. (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiology 107, 207-213.
21. Dougall D.K., Labrake S. & Whitten G.H. (1983) The effects of limiting nutrients, dilution rate, culture pH, and temperature on the yield constant and anthocyanin accumulation of carrot cells grown in semicontinuous chemostat cultures. Biotechnology and Bioengineering 25, 569-579.
22. Erban A., Schauer N., Fernie A.R. & Kopka J. (2007) Non-supervised construction and application of mass spectral and retention time index libraries from time-of-flight GC-MS metabolite profiles. Methods in Molecular Biology 358, 19-38.
23. Fiehn O., Kopka J., Dörmann P., Altmann T., Trethewey R.N. & Willmitzer L. (2000) Metabolite profiling for plant functional genomics. Nature Biotechnology 18, 1157-1161.
24. Fixen P.E. (2009) World fertilizer nutrient reserves - a view to the future. The Better Crops 93, 8-11.
25. Fixen P.E. & Johnston A.M. (2012) World fertilizer nutrient reserves: a view to the future. Journal of the Science of Food and Agriculture 92, 1001-1005.
26. Fredeen A.L., Raab T.K., Rao M. & Terry N. (1990) Effects of phosphorus nutrition on photosynthesis in Glycine max. (L.) Merr. Planta 181, 399-405.
27. Gallego-Giraldo L., Escamilla-Trevino L., Jackson L.A. & Dixon R.A. (2011) Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proceedings of the National Academy of Sciences of the United States of America 108, 20814-20819.
28. Gaude N., Nakamura Y., Scheible W.R., Ohta H. & Dörmann P. (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. The Plant Journal: For Cell and Molecular Biology 56, 28-39.
29. Giersch C. & Robinson S.P. (1987) Regulation of photosynthetic carbon metabolism during phosphate limitation of photosynthesis in isolated spinach chloroplasts. Photosynthesis Research 14, 211-227.
30. Guo F.Q., Okamoto M. & Crawford N.M. (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100-103.
31. Hell R. (1997) Molecular physiology of plant sulfur metabolism. Planta 202, 138-148.
32. Hernandez G., Ramirez M., Valdes-Lopez O., Tesfaye M., Graham M.A., Czechowski T., ... Vance C.P. (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiology 144, 752-767.
33. Hernandez G., Valdes-Lopez O., Ramirez M., Goffard N., Weiller G., Aparicio-Fabre R., ... Vance C.P. (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiology 151, 1221-1238.
34. Hewitt M.M., Carr J.M., Williamson C.L. & Slocum R.D. (2005) Effects of phosphate limitation on expression of genes involved in pyrimidine synthesis and salvaging in Arabidopsis. Plant Physiology and Biochemistry 43, 91-99.
35. Hummel J., Strehmel N., Selbig J., Walther D. & Kopka J. (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics: Official Journal of the Metabolomic Society 6, 322-333.
36. Hurley B.A., Tran H.T., Marty N.J., Park J., Snedden W.A., Mullen R.T. & Plaxton W.C. (2010) The dual-targeted purple acid phosphatase isozyme AtPAP26 is essential for efficient acclimation of Arabidopsis to nutritional phosphate deprivation. Plant Physiology 153, 1112-1122.
37. Hurry V., Strand A., Furbank R. & Stitt M. (2000) The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. The Plant Journal: For Cell and Molecular Biology 24, 383-396.
38. Itaya K. & Ui M. (1966) A new micromethod for the colorimetric determination of inorganic phosphate. Clinica Chimica Acta 14, 361-366.
39. Jacob J. & Lawlor D.W. (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. Journal of Experimental Botany 42, 1003-1011.
40. Jacob J. & Lawlor D.W. (1993) Extreme phosphate deficiency decreases the in vivo CO2/O2 specificity factor of ribulose 1, 5-bisphosphate carboxylase-oxygenase in intact leaves of sunflower. Journal of Experimental Botany 44, 1635-1641.
41. Johnson J.F., Vance C.P. & Allan D.L. (1996) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiology 112, 31-41.
42. Kim J.H. & Jander G. (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. The Plant Journal: For Cell and Molecular Biology 49, 1008-1019.
43. Kondracka A. & Rychter A.M. (1997) The role of Pi recycling processes during photosynthesis in phosphate-deficient bean plants. Journal of Experimental Botany 48, 1461-1468.
44. Kopka J., Schauer N., Krueger S., Birkemeyer C., Usadel B., Bergmüller E., ... Steinhauser D. (2005) GMD@CSB.DB: the Golm Metabolome database. Bioinformatics (Oxford, England) 21, 1635-1638.
45. Lam H.M., Coschigano K.T., Oliveira I.C., Melo-Oliveira R. & Coruzzi G.M. (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 569-593.
46. Lambers H., Finnegan P.M., Laliberte E., Pearse S.J., Ryan M.H., Shane M.W. & Veneklaas E.J. (2011) Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiology 156, 1058-1066.
47. Lambers H., Cawthray G.R., Giavalisco P., Kuo J., Laliberte E., Pearse S.J., ... Turner B.L. (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. The New Phytologist 196, 1098-1108.
48. Li D., Zhu H., Liu K., Liu X., Leggewie G., Udvardi M. & Wang D. (2002) Purple acid phosphatases of Arabidopsis thaliana. Comparative analysis and differential regulation by phosphate deprivation. The Journal of Biological Chemistry 277, 27772-27781.
49. Li M., Welti R. & Wang X. (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases D zeta1 and D zeta2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiology 142, 750-761.
50. Linka M. & Weber A.P. (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends in Plant Science 10, 461-465.
51. Lisec J., Schauer N., Kopka J., Willmitzer L. & Fernie A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387-396.
52. López-Berenguer C., Martínez-Ballesta M.C., García-Viguera C. & Carvajal M. (2008) Leaf water balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in broccoli. The Plant Science 174, 321-328.
53. 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 Physiology 129, 244-256.
54. Luedemann A., Strassburg K., Erban A. & Kopka J. (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics (Oxford, England) 24, 732-737.
55. Lynch J.P. (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156, 1041-1049.
56. McNear D.H. Jr. (2013) The rhizosphere - roots, soil and everything in between. Nature Education Knowledge 4, 1.
57. Marschner M. (1995) Mineral Nutrition of Higher Plants, 2nd edn, Academic Press Limited, London, UK.
58. Martinez C., Pons E., Prats G. & Leon J. (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. The Plant Journal: For Cell and Molecular Biology 37, 209-217.
59. Masclaux-Daubresse C., Daniel-Vedele F., Dechorgnat J., Chardon F., Gaufichon L. & Suzuki A. (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 1141-1157.
60. Misson J., Raghothama K.G., Jain A., Jouhet J., Block M.A., Bligny R., ... Thibaud M.C. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences of the United States of America 102, 11934-11939.
61. Morcuende R., Bari R., Gibon Y., Zheng W., Pant B.D., Bläsing O., ... Scheible W.R. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell and Environment 30, 85-112.
62. Morris K., MacKerness S.A., Page T., John C.F., Murphy A.M., Carr J.P. & Buchanan-Wollaston V. (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. The Plant Journal: For Cell and Molecular Biology 23, 677-685.
63. Nilsson L., Müller R. & Nielsen T.H. (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant, Cell and Environment 30, 1499-1512.
64. Nilsson L., Lundmark M., Jensen P.E. & Nielsen T.H. (2012) The Arabidopsis transcription factor PHR1 is essential for adaptation to high light and retaining functional photosynthesis during phosphate starvation. Physiologia Plantarum 144, 35-47.
65. Nishizawa A., Yabuta Y. & Shigeoka S. (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology 147, 1251-1263.
66. Pang Y., Wenger J.P., Saathoff K., Peel G.J., Wen J., Huhman D., ... Dixon R.A. (2009) A WD40 repeat protein from Medicago truncatula is necessary for tissue-specific anthocyanin and proanthocyanidin biosynthesis but not for trichome development. Plant Physiology 151, 1114-1129.
67. Pant B.D., Buhtz A., Kehr J. & Scheible W.-R. (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal 53, 731-738.
68. Pant B.D., Musialak-Lange M., Nuc P., May P., Buhtz A., Kehr J., ... Scheible W.R. (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150, 1541-1555.
69. Pérez-Balibrea S., Moreno D.A. & García-Viguera C. (2008) Influence of light on health promoting phytochemicals of broccoli sprouts. Journal of the Science of Food and Agriculture 88, 904-910.
70. Plaxton W.C. (1996) The organization and regulation of plant glycolysis. Annual Review of Plant Physiology and Plant Molecular Biology 47, 185-214.
71. Plaxton W.C. & Tran H.T. (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiology 156, 1006-1015.
72. Poirier Y. & Bucher M. (2002) Phosphate transport and homeostasis in Arabidopsis. The Arabidopsis Book [electronic resource] / American Society of Plant Biologists 1, e0024.
73. Qin L., Zhao J., Tian J., Chen L.Y., Sun Z.A., Guo Y.X., ... Liao H. (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiology 159, 1634-1643.
74. Rabe E. & Lovatt C.J. (1986) Increased arginine biosynthesis during phosphorus deficiency : a response to the increased ammonia content of leaves. Plant Physiology 81, 774-779.
75. Raghothama K.G. (1999) Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50, 665-693.
76. Ramakrishna A. & Ravishankar G.A. (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling and Behavior 6, 1720-1731.
77. Rao I.M. & Terry N. (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet (IV. Changes with time following increased supply of phosphate to low-phosphate plants). Plant Physiology 107, 1313-1321.
78. Roessner U., Wagner C., Kopka J., Trethewey R.N. & Willmitzer L. (2000) Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. The Plant Journal: For Cell and Molecular Biology 23, 131-142.
79. Rouached H., Stefanovic A., Secco D., Bulak Arpat A., Gout E., Bligny R. & Poirier Y. (2011) Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant Journal 65, 557-570.
80. 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 and Development 15, 2122-2133.
81. Rufty T.W., Mackown C.T. & Israel D.W. (1990) Phosphorus stress effects on assimilation of nitrate. Plant Physiology 94, 328-333.
82. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., ... Quackenbush J. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378.
83. Saeed A.I., Bhagabati N.K., Braisted J.C., Liang W., Sharov V., Howe E.A., ... Quackenbush J. (2006) TM4 microarray software suite. Methods in Enzymology 411, 134-193.
84. Schauer N., Steinhauser D., Strelkov S., Schomburg D., Allison G., Moritz T., ... Kopka J. (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Letters 579, 1332-1337.
85. Schlesier B., Breton F. & Mock H.P. (2003) A hydroponic culture system for growing Arabidopsis thaliana plantlets under sterile conditions. Plant Molecular Biology Reporter 21, 449-456.
86. Scholz M., Kaplan F., Guy C.L., Kopka J. & Selbig J. (2005) Non-linear PCA: a missing data approach. Bioinformatics (Oxford, England) 21, 3887-3895.
87. Secco D., Jabnoune M., Walker H., Shou H., Wu P., Poirier Y. & Whelan J. (2013) Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. The Plant Cell 25, 4285-4304.
88. Seigler D.S. (1998) Plant Secondary Metabolism, Chapman and Hall, Boston, MA, USA.
89. Shaff J.E., Schultz B.A., Craft E.J., Clark R.T. & Kochian L.V. (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant and Soil 330, 207-214.
90. Shane M.W., Cramer M.D., Funayama-Noguchi S., Cawthray G.R., Millar A.H., Day D.A. & Lambers H. (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiology 135, 549-560.
91. Strehmel N., Hummel J., Erban A., Strassburg K. & Kopka J. (2008) Retention index thresholds for compound matching in GC-MS metabolite profiling. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 871, 182-190.
92. Sulpice R., Ishihara H., Schlereth A., Cawthray G.R., Encke B., Giavalisco P., ... Lambers H. (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant, Cell and Environment 37, 1276-1298.
93. Taylor C.B., Bariola P.A., delCardayre S.B., Raines R.T. & Green P.J. (1993) RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proceedings of the National Academy of Sciences of the United States of America 90, 5118-5122.
94. Thimm O., Bläsing O., Gibon Y., Nagel A., Meyer S., Kruger P., ... Stitt M. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal: For Cell and Molecular Biology 37, 914-939.
95. Tohge T., Nishiyama Y., Hirai M.Y., Yano M., Nakajima J., Awazuhara M., ... Saito K. (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. The Plant Journal: For Cell and Molecular Biology 42, 218-235.
96. Vaccari D.A. (2009) Phosphorus: a looming crisis. Scientific American 300, 54-59.
97. Van den Ende W., De Coninck B. & Van Laere A. (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends in Plant Science 9, 523-528.
98. Van Kauwenbergh S.J., Stewart M. & Mikkelsen R. (2013) World reserves of phosphate rock... a dynamic and unfolding story. The Better Crops 97, 18-20.
99. Veneklaas E.J., Lambers H., Bragg J., Finnegan P.M., Lovelock C.E., Plaxton W.C., ... Raven J.A. (2012) Opportunities for improving phosphorus-use efficiency in crop plants. The New Phytologist 195, 306-320.
100. Wagner C., Sefkow M. & Kopka J. (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry 62, 887-900.
101. Wasaki J., Yonetani R., Kuroda S., Shinano T., Yazaki J., Fujii F., ... Osaki M. (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant, Cell and Environment 26, 1515-1523.
102. Williamson L.C., Ribrioux S.P., Fitter A.H. & Leyser H.M. (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology 126, 875-882.
103. Woo J., MacPherson C.R., Liu J., Wang H., Kiba T., Hannah M.A., ... Chua N.H. (2012) The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation. BMC Plant Biology 12, 62.
104. Wu P., Ma L.G., Hou X.L., Wang M.Y., Wu Y.R., Liu F.Y. & Deng X.W. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiology 132, 1260-1271.
105. Zhang H., Schonhof I., Krurnbein A., Gutezeit B., Li L., Stuzel H. & Schreiner M. (2008) Water supply and growing season influence glucosinolate concentration and composition in turnip root (Brassica rapa ssp rapifera L.). Journal of Plant Nutrition and Soil Science 171, 255-265.
106. Zhang P., Dreher K., Karthikeyan A., Chi A., Pujar A., Caspi R., ... Rhee S.Y. (2010) Creation of a genome-wide metabolic pathway database for Populus trichocarpa using a new approach for reconstruction and curation of metabolic pathways for plants. Plant Physiology 153, 1479-1491.
107. Zrenner R., Stitt M., Sonnewald U. & Boldt R. (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annual Review of Plant Biology 57, 805-836.