Nutrient sensing and signaling: NPKS

Annual Review of Plant Biology

Volumn 58, Issue , 2007, Pages 47-69

  Schachtman, Daniel P ^a   Shin, Ryoung ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

Nitrogen; Nutrient deprivation; Phosphorus; Potassium; Sulfur

Indexed keywords

NITROGEN; PHOSPHORUS; POTASSIUM; REACTIVE OXYGEN METABOLITE; SULFUR;

ADAPTATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT; REVIEW; SIGNAL TRANSDUCTION; TIME;

ADAPTATION, PHYSIOLOGICAL; NITROGEN; PHOSPHORUS; PLANTS; POTASSIUM; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SULFUR; TIME FACTORS;

EID: 34347262497     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.58.032806.103750     Document Type: Review

References (156)

1. Abel S, Ticconi CA, Delatorre CA. 2002. Phosphate sensing in higher plants. Physiol. Plant 115:1-8
2. + uptake. Plant Physiol. 134:1135-45
3. Amtmann A, Hammond J, Armenguad P, White PJ. 2006. Nutrient sensing and signaling in plants: potassium and phosphorus. Adv. Bot. Res. 43:209-57
4. Armengaud P, Breitling R, Amtmann A. 2004. The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol. 136:2556-76
5. Ashley MK, Grant M, Grabov A. 2006. Plant responses to potassium deficiencies: a role for potassium transport proteins. J. Exp. Bot. 57:425-36
6. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ. 2006. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141:1000-11
7. Awazuhara M, Kima H, Goto DB, Matsui A, Hayashi H, et al. 2002. A 235-bp region from a nutritionally regulated soybean seed-specific gene promoter can confer its sulfur and nitrogen response to a constitutive promoter in aerial tissues of Arabidopsis thaliana. Plant Sci. 163:75-82
8. Baldwin JC, Karthikeyan AS, Raghothama KG. 2001. LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol. 125:728-37
9. Bari R, Datt Pant B, Stitt M, Scheible WR. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141:988-99
10. Blake-Kalff MMA, Harrison KR, Hawkesford MJ, Zhao FJ, McGrath SP. 1998. Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth. Plant Physiol. 118:1337-44
11. Bloom AJ, Finazzo J. 1986. The influence of ammonium and chloride on potassium and nitrate absorption by barley roots depend on time of exposure and cultivar. Plant Physiol. 81:67-69
12. Burleigh SH, Harrison MJ. 1999. The down-regulation of Mt4-like genes by phosphate fertilization occurs systematically and involves phosphate translocation to the shoots. Plant Physiol. 119:241-48
13. Carswell C, Grant BR, Theodorou ME, Harris J, Niere JO, Plaxton WC. 1996. The fungicide phosphonate disrupts the phosphate-starvation response in Brassica nigra seedlings. Plant Physiol. 110:105-10
14. Carswell MC, Grant BR, Plaxton WC. 1997. Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide phosphonate. Planta 203:67-74
15. Chen YM, Ferrar TS, Lohmeir-Vogel E, Morrice N, Mizuno Y, et al. 2006. The PII signal transduction protein of Arabidopsis thaliana forms an arginine-regulated complex with plastid N-acetyl glutamate kinase. J. Biol. Chem. 281:5726-33
16. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL. 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412-21
17. Coello P, Polacco JC. 1999. ARR6, a response regulator from Arabidopsis, is differentially regulated by plant nutritional status. Plant Sci. 143:211-20
18. Conklin PL, Barth C. 2004. Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ. 27:959-70
19. Davies JP, Yildiz FH, Grossman AR. 1999. Sac3, an snf1-like serine/threonine kinase that positively and negatively regulates the responses of Chlamydomonas to sulfur limitation. Plant Cell 11:1179-90
20. Delhaize E, Randall PJ. 1995. Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 107:207-13
21. Demidchik V, Essah PA, Tester M. 2004. Glutamate activates cation currents in the plasma membrane of Arabidopsis root cells. Planta 219:167-75
22. Dunlop J, Gardiner S. 1993. Phosphate uptake, proton extrusion and membrane electropotentials of phosphorus-deficient Trifolium repens L. J. Exp. Bot. 44:1801-8
23. Fan M, Zhu J, Richards C, Brown KM, Lynch JP. 2003. Physiological roles for aerenchyma in phosphorus-stressed roots. Funct. Plant Biol. 30:493-506
24. Ferrario-Mery S, Besin E, Pichon O, Meyer C, Hodges M. 2006. The regulatory PII protein controls arginine biosynthesis in Arabidopsis. FEBS Lett. 580:2015-20
25. Filleur S, Walch-Liu P, Gan Y, Forde BG. 2005. Nitrate and glutamate sensing by plant roots. Biochem. Soc. Trans. 33:283-86
26. Forde BG. 2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol. 53:203-24
27. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-46
28. 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. 55:285-93
29. 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. 138:847-57
30. 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. 32:353-60
31. Fu H, Dooner HK. 2002. Intraspecific violation of genetic colinearity and its implications in maize. Proc. Natl. Acad. Sci. USA 99:9573-78
32. Fu Y, Paietta J, Mannix D, Marzluf G. 1989. Cys-3, the positive-acting sulfur regulatory gene of Neurospora crassa, encodes a protein with a putative leucine zipper DNA-binding element. Mol. Cell. Biol. 9:1120-27
33. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15:2038-43
34. Gallais A, Hirel B. 2004. An approach to the genetics of nitrogen use efficiency in maize. J. Exp. Bot. 55:295-306
35. Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG. 2005. Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222:730-42
36. + uptake kinetics in Arabidopsis roots. Plant Physiol. 137:1105-14
37. Gilbert SM, Clarkson DT, Cambridge M, Lambers H, Hawkesford MJ. 1997. Sulfate-deprivation has an early effect on the content of ribulose 1,5-bisphosphate carboxylase/ oxygenase and photosynthesis in young leaves of wheat. Plant Physiol. 115:1231-39
38. Gonzalez E, Solano R, Rubio V, Leyva A, Paz-Ares J. 2005. PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500-12
39. Good AG, Shrawat AK, Muench DG. 2004. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci. 9:597-605
40. Grime J. 1977. Evidence for the existence of three primary stategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111:1169-94
41. Gyaneshwar P, Paliy O, McAuliffe J, Jones A, Jordan M, Kustu S. 2005. Lesson from Escherichia coli genes similarly regulated in response to nitrogen and sulfur limitation. Proc. Natl. Acad. Sci. USA 102:3453-58
42. Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, et al. 2003. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 132:578-96
43. Handreck K. 1997. Phosphorus requirements of Australian native plants. Aust. J. Soil Res. 35:241-89
44. Hesse H, Nikiforova V, Gakiere B, Hoefgen R. 2004. Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. J. Exp. Bot. 55:1283-92
45. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K. 2003. Global expression profiling of sulfur-starved Arabidopsis by DNA microarray reveals the role of O-acetyl-1-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33:651-63
46. Hirai MY, Saito K. 2004. Post-genomics approaches for the elucidation of plant adaptive mechanisms to sulphur deficiency. J. Exp. Bot. 55:1871-79
47. Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, et al. 2004. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101:10205-10
48. Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol. 162:9-24
49. Horgan J, Wareing P. 1980. Cytokinins and the growth responses of seedlings of Beula pendula Roth, and Acer pseudoplatanus L. to nitrogen and phosphorus deficiency. J. Exp. Bot. 31:525-32
50. Hsieh MH, Lam HM, van de Loo FJ, Coruzzi G. 1998. A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc. Natl. Acad. Sci. USA 95:13965-70
51. Hwang I, Sheen J. 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383-89
52. Irihimovitch V, Stern DB. 2006. The sulfur acclimation SAC3 kinase is required for chloroplast transcriptional repression under sulfur limitation in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103:7911-16
53. Jones-Rhoades MW, Bartel DP. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14:787-99
54. Jost R, Altschmied L, Bloem E, Bogs J, Gershenzon J, et al. 2005. Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana. Photosynthesis Res. 86:491-508
55. + and ionic strength directly influence the autophosphorylation activity of the putative turgor sensor KdpD of Escherichia coli. J.Biol. Chem. 275:40142-47
56. Kaiser WM, Huber SC. 2001. Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J. Exp. Bot. 52:1981-89
57. Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz KJ. 2004. The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol. Plant. 120:63-73
58. Kang JM, Turano FJ. 2003. The putative glutamate receptor 1.1 (AtGLR11) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100:6872-77
59. 2+ binding motifs. Plant Cell 10:255-66
60. Konings H, Verschuren G. 1980. Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiol. Plant. 49:265-70
61. Kopriva S. 2006. Regulation of sulfate assimilation in Arabidopsis and beyond. Annals. Bot. 97:479-95
62. Kumar A, Paietta J. 1995. The sulfur controller-2 negative regulatory gene of Neurospora crassa encodes a protein with β-transduction repeats. Proc. Natl. Acad. Sci. USA 92:3343-47
63. Kumar A, Paietta JV. 1998. An additional role for the F-box motif: gene regulation within the Neurospora crassa sulfur control network. Proc. Natl. Acad. Sci. USA 95:2417-22
64. Kuras L, Cherest H, Surdin-Kerjan Y, Thomas D. 1996. A heteromeric complex containing the centromere binding factor1 and two basic leucine zipper factors, Met4 and Met28, mediates the transcription activation of yeast sulfur metabolism. EMBO J. 15:2519-29
65. Kutz A, Müller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW. 2002. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J. 30:95-106
66. Lacombe B, Becker D, Hedrich R, DeSalle R, Hollmann M, et al. 2001. The identity of plant glutamate receptors. Science 292:1486-87
67. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-75
68. 2- uptake and oxidative stress response in intact canola roots. Plant Physiol. 114:177-83
69. Lejay L, Tillard P, Lepetit M, Olive F, Filleur S, et al. 1999. Molecular and functional regulation of two NO3- uptake systems by N- and C-status of Arabidopsis plants. Plant J. 18:509-19
70. Lencioni L, Ranieri A, Fergola S, Soldatini G. 1997. Photosynthesis and metabolic changes in leaves of rapeseed grown under long-term sulfate deprivation. J. Plant Nutr. 20:405-15
71. Leustek T, Martin MN, Bick JA, Davies JP. 2000. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:141-65
72. Leustek T, Saito K. 1999. Sulfate transport and assimilation in plants. Plant Physiol. 120:637-44
73. + channel for low-K response in Arabidopsis. Proc. Natl. Acad. Sci. USA 103:12625-30
74. Li M, Qin C, Welti R, Wang X. 2006. Double knockouts of phospholipases Dz1 and Dz2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol. 140:761-70
75. Linkohr BI, Williamson LC, Fitter AH, Leyser HM. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J. 29:751-60
76. 2, and OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 136:3114-23
77. Little DY, Rao H, Oliva S, Daniel-Vedele F, Krapp A, Malamy JE. 2005. The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl. Acad. Sci. USA 102:13693-98
78. Liu KH, Tsay YF. 2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22:1005-13
79. López-Bucio J, Cruz-Ramirez A, Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6:280-87
80. López-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. 129:244-56
81. Ma Z, Bielenberg DG, Brown KM, Lynch JP. 2001. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 24:459-67
82. Maathuis FJ, Filatov V, Herzyk P, Krijger G, Axelsen K, et al. 2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J. 35:675-92
83. Mallory AC, Vaucheret H. 2006. Functions of microRNAs and related small RNAs in plants. Nat. Genet. 38 Suppl 1:S31-36
84. Marschner H. 1995. Mineral Nutrition of Higher Plants. San Diego: Academic. 889p.
85. Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, et al. 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 24:559-67
86. Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H. 2003. Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132:597-605
87. th, Madison, Wis.
88. Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H. 2005. Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J. 42:305-14
89. Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Yamaya T, Takahashi H. 2004. Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol. 45:340-45
90. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H. 2004. Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signaling and regulation. J. Exp. Bot. 55:1843-49
91. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H. 2004. A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 38:779-89
92. Migge A, Bork C, Hell R, Becker T. 2000. Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco. Planta 211:587-95
93. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, et al. 2005. A genomewide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. USA 102:11934-39
94. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, et al. 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. USA 102:7760-65
95. Miyake K, Ito T, Senda M, Ishikawa R, Harada T, et al. 2003. Isolation of a subfamily of genes for R2R3-MYB transcription factors showing up-regulated expression under nitrogen nutrient-limited conditions. Plant Mol. Biol. 53:237-45
96. Moorhead GB, Smith CS. 2003. Interpreting the plastid carbon, nitrogen, and energy status. A role for PII? Plant Physiol. 133:492-98
97. 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypotheticalfy mechanotransduction. Plant Physiol. 135:702-8
98. Mostertz J, Scharf C, Hecker M, Homuth G. 2004. Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiol. 150:497-512
99. Mukatira UT, Liu C, Varadarajan DK, Raghothama KG. 2001. Negative regulation of phosphate starvation-induced genes. Plant Physiol. 127:1854-62
100. Muller S, Hoege C, Pyrowolakis G, Jentsch S. 2001. SUMO, Ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2:202-10
101. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, et al. 2005. A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol. 138:2061-74
102. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R. 2003. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interacting of biosynthetic pathways provides response specificity. Plant J. 33:633-50
103. Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, et al. 2005. Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol. 138:304-18
104. Ohkama N, Takei K, Sakakibara H, Hayashi H, Yoneyama T, Fujiwara T. 2002. Regulation of sulfur-responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol. 43:1493-501
105. Paietta J. 1992. Production of the CYS3 regulator, a bZIP DNA-binding protein, is sufficient to induce sulfur gene expression in Neurospora crassa. Mol. Cell. Biol. 12:1568-77
106. Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM. 2004. Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol. 5:R91
107. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, et al. 2003. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939-51
108. + channel expression represents an essential step in coleoptile growth and gravitropism. Proc. Natl. Acad. Sci. USA 96:12186-91
109. Prosser I, Purves J, Saker L, Clarkson D. 2001. Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J. Exp. Bot. 52:113-21
110. Ravina CG, Chang CI, Tsakraklides GP, McDermott JP, Vega JM, et al. 2002. The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol. 130:2076-84
111. Remans T, Nacry P, Pervent M, Girin T, Tillard P, et al. 2006. A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol. 140:909-21
112. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, et al. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15:2122-33
113. Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281-90
114. Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57:431-49
115. Sakakibara H, Suzuki M, Takei K, Deji A, Taniguchi M, Sugiyama T. 1998. A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 14:337-44
116. Sanchez P. 2002. Soil fertility and hunger in Africa. Science 295:2019-20
117. Sano H, Youssefian S. 1994. Light and nutritional regulation of transcripts encoding a wheat protein kinase homolog is mediated by cytokinins. Proc. Natl. Acad. Sci. USA 91:2582-86
118. Santa-Maria GE, Danna CH, Czibener C. 2000. High-affinity potassium transport in barley roots. Ammonium-sensitive and -insensitive pathways. Plant Physiol. 123:297-306
119. Schachtman DP, Reid RJ, Ayling SM. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116:447-53
120. Scheible WR, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M. 1997. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783-98
121. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, et al. 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136:2483-99
122. Schunmann PH, Richardson AE, Vickers CE, Delhaize E. 2004. Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol. 136:4205-14
123. Setya A, Murillo M, Leustek T. 1996. Sulfate reduction in higher plants: molecular evidence for a novel 5-adenylylsulfate reductase. Proc. Natl. Acad. Sci. USA 93:13383-88
124. Shin H, Shin HS, Chen R, Harrison MJ. 2006. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J. 45:712-26
125. Shin R, Berg RH, Schachtman DP. 2005. Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol. 46:1350-57
126. Shin R, Schachtman DP. 2004. Hydrogen peroxide mediates plant root response to nutrient deprivation. Proc. Natl. Acad. Sci. USA 101:8827-32
127. Smith F, Ealing P, Hawkesford M, Clarkson D. 1995. Plant members of a family of sulfate transporters reveal functional subtypes. Proc. Natl. Acad. Sci. USA 92:9373-77
128. Spalding EP, Hirsch RE, Lewis DR, Qi Z, Sussman MR, Lewis BD. 1999. Potassium uptake supporting plant growth in the absence of AKT1 channel activity. J. Gen. Phsyiol. 113:909-18
129. Stitt M, Muller C, Matt P, Gibon Y, Carillo P, et al. 2002. Steps towards an integrated view of nitrogen metabolism. J. Exp. Bot. 53:959-70
130. Sugiharto B, Suzuki I, Burnell JN, Sugiyama T. 1992. Glutamine induces the N-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol. 100:2066-70
131. Sugiura A, Hirokawa K, Nakashima K, Mizuno T. 1994. Signal-sensing mechanisms of the putative osmosensor KdpD in Escherichia coli. Mol. Microbiol. 14:929-38
132. Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K. 2000. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23:171-82
133. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, et al. 1997. Regulation of sulfur assimilation in higher plants: A sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94:11102-7
134. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H. 2002. Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J. Exp. Bot. 53:971-77
135. Taniguchi M, Kiba T, Sakakibara H, Ueguchi C, Mizuno T, Sugiyama T. 1998. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429:259-62
136. Thanos D, Maniatis T. 1995. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 83:1091-100
137. Thomas D, Kuras L, Barbey R, Cherest H, Blaiseau P, Surdin-Kerjan Y. 1995. Met30p, a yeast transcriptional inhibitor that responds to S-adenosylmethionine, is an essential protein with WD40 repeats. Mol. Cell. Biol. 15:6526-34
138. Ticconi CA, Abel S. 2004. Short on phosphate: plant surveillance and countermeasures. Trends Plant. Sci. 9:548-55
139. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S. 2004. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J. 37:801-14
140. Todd CD, Zeng P, Huete AM, Hoyos ME, Polacco JC. 2004. Transcripts of MYB-like genes respond to phosphorus and nitrogen deprivation in Arabidopsis. Planta 219:1003-9
141. Torres MA, Dangl JL. 2005. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8:397-403
142. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, et al. 2003. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl. Acad. Sci. USA 100:16113-18
143. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A. 2004. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J. 40:523-35
144. Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG. 2006. Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol. 47:1045-57
145. Walderhaug MO, Polarek JW, Voelkner P, Daniel JM, Hesse JE, et al. 1992. KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J. Bacteriol. 174:2152-59
146. Wang R, Guegler K, LaBrie ST, Crawford NM. 2000. Genomic analysis of nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491-509
147. Wang R, Okamoto M, Xing X, Crawford NM. 2003. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 132:556-67
148. Wang X. 2005. Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiol. 139:566-73
149. Wang YH, Garvin DF, Kochian LV. 2001. Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol. 127:345-59
150. 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. 130:1361-70
151. Wilkinson S, Davies WJ. 2002. ABA-based chemical signaling: the co-ordination of responses to stress in plants. Plant Cell Environ. 25:195-210
152. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM. 2001. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol. 126:875-82
153. Wilson WA, Roach PJ. 2002. Nutrient-regulated protein kinases in budding yeast. Cell 111:155-58
154. Xiang C, Oliver D. 1998. Glutatione metabolic genes cordinately respond to heavy metals and jasmoic acid in Arabidopsis. Plant Cell 10:1539-50
155. + transporter AKT1 in Arabidopsis. Cell 125:1347-60
156. Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. 2002. Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29:465-73