Nitrogen acquisition by roots: Physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource

Plant and Soil

Volumn 370, Issue 1-2, 2013, Pages 1-29

  Nacry, Philippe ^a   Bouguyon, Eléonore ^a   Gojon, Alain ^a  

^a MONTPELLIER SUPAGRO   (France)

Author keywords

Ammonium; Nitrate; Nutrient sensing and signalling; Root development; Root uptake; Urea

Indexed keywords

ADAPTATION; CONCENTRATION (COMPOSITION); HOMEOSTASIS; NITROGEN CYCLE; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; PHYSIOLOGY; PLANT COMMUNITY; ROOT SYSTEM; SOIL NUTRIENT; SPATIOTEMPORAL ANALYSIS;

ARABIDOPSIS THALIANA;

EID: 84873969262     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-013-1645-9     Document Type: Review

References (232)

1. Alvarez JM, Vidal EA, Gutiérrez RA (2012) Integration of local and systemic signaling pathways for plant N responses. Curr Opin Plant Biol 15: 185-191.
2. Amarasinghe BH, de Bruxelles GL, Braddon M, Onyeocha I, Forde BG, Udvardi MK (1998) Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max). Planta 206: 44-52.
3. Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F, Thomine S, Wege S (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62: 25-51.
4. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
5. + supply modifies the root system architecture of Cedrus atlantica seedlings grown in a split-root device. J Plant Physiol 163: 1293-1304.
6. Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44: 314-333.
7. Brewitz E, Larsson C-M, Larsson M (1995) Influence of nitrate supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Phvsiol Plant 95: 499-506.
8. Burns IG (1991) Short and long term effects of a change in the spatial distribution of nitrate in the root zone on N uptake, growth and root development of young lettuce plants. Plant Cell Environ 14: 21-23.
9. Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211: 98-104.
10. Cai C, Wang JY, Zhu YG, Shen QR, Li B, Tong YP, Li ZS (2008) Gene structure and expression of the high-affinity nitrate transport system in rice roots. J Integr Plant Biol 50: 443-451.
11. Camanes G, Cerezo M, Primo-Millo E, Gojon A, Garcia-Agustin P (2007) Ammonium transport and CitAMT1 expression are regulated by light and sucrose in Citrus plants. J Exp Bot 58: 2811-2825.
12. Camargo A, Llamas A, Schnell RA, Higuera JJ, González-Ballester D, Lefebvre PA, Fernández E, Galván A (2007) Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19: 3491-3503.
13. Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth's nitrogen cycle. Science 330: 192-196.
14. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57: 426-435.
15. - uptake are associated with the mutation of Nrt2. 1 and Nrt2. 2 genes in Arabidopsis. Plant Physiol 127: 262-271.
16. Chapin FS (1991) Integrated responses of plants to stress. Bioscience 41: 29-36.
17. Chapin FS, Clarkson DT, Lenton LR, Walter CHS (1988) Effect of nitrogen stress and abscissic acid on nitrate absorption and transport in barley and tomato. Planta 173: 340-351.
18. Chapman N, Whalley WR, Lindsey K, Miller AJ (2011) Water supply and not nitrate concentration determines primary root growth in Arabidopsis. Plant Cell Environ 34: 1630-1638.
19. Chiou TJ, Aung K, Lin S, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412-421.
20. Chun L, Mi GH, Li JS, Chen FJ, Zhang FS (2005) Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant Soil 276: 369-382.
21. Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Ann Rev Plant Physiol 36: 77-115.
22. Cooper HD, Clarkson DT (1989) Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals- A possible mechanism integrating shoot and root in the regulation of nutrient uptake. J Exp Bot 40: 753-762.
23. Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7: 859-868.
24. Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3: 389-395.
25. D'Apuzzo E, Rogato A, Simon-Rosin U, El Alaoui H, Barbulova A, Betti M, Dimou M, Katinakis P, Marquez A, Marini AM, Udvardi MK, Chiurazzi M (2004) Characterization of three functional high-affinity ammonium transporters in Lotus japonicus with differential transcriptional regulation and spatial expression. Plant Physiol 134: 1763-1774.
26. Datko AH, Mudd SH (1985) Uptake of amino acids and other organic compounds by Lemna paucicostata Hegelm. 6746. Plant Physiol 77: 770-778.
27. De Kroon H, Visser EJ, Huber H, Mommer L, Hutchings MJ (2009) A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ 32: 704-712.
28. De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33: 543-555.
29. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321: 926-929.
30. Doddema H, Telkamp GP (1979) Uptake of nitrate by mutants of Arabidopsis thaliana disturbed in uptake or reduction of nitrate. II. Kinetics. Physiol Plant 45: 332-338.
31. Drew MC (1975) Comparison of effects of a localized supply of phosphate, nitrate, ammonium and potassium on growth of seminal root system and shoot in barley. New Phytol 75: 479-490.
32. Engelsberger WR, Schulze WX (2012) Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings. Plant J 69: 978-995.
33. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9-19.
34. Feng H, Yan M, Fan X, Li B, Shen Q, Miller AJ, Xu G (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J Exp Bot 62: 2319-2332.
35. Filleur S, Daniel-Vedele F (1999) Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207: 461-469.
36. Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F, Gojon A, Daniel-Vedele F (2001) An arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett 489: 220-224.
37. Filleur S, Walch-Liu P, Gan Y, Forde BG (2005) Nitrate and glutamate sensing by plant roots. Biochem Soc Trans 33: 283-286.
38. Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta 1465: 219-235.
39. Forde BG (2002) Local and long-range signalling pathways regulating plant responses to nitrate. Ann Rev Plant Biol 53: 203-224.
40. Forde BG, Clarkson DT (1999) Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv Bot Res 30: 1-90.
41. Fraisier V, Gojon A, Tillard P, Daniel-Vedele F (2000) Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source. Plant J 23: 489-496.
42. Fransen B, de Kroon H, Berendse F (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115: 351-358.
43. Frommer WB, Hummel S, Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc Natl Acad Sci USA 90: 5944-5948.
44. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. BioScience 53: 341-356.
45. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878): 889-892.
46. Gan Y, Bernreiter A, Filleur S, Abram B, Forde BG (2012) Over-expressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol 53: 1003-1016.
47. + transporter genes AtNrt2. 1 and AtAmt1. 1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. Plant J 26: 143-155.
48. Gazzarini S, Lejay L, Gojon A, Ninnemann O, Frommer WB (1999) Three functional transporters for constitutive, diurnally regulated and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11: 937-947.
49. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106: 21425-21430.
50. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105: 803-808.
51. Girin T, Lejay L, Wirth J, Widiez T, Palenchar PM, Nazoa P, Touraine B, Gojon A, Lepetit M (2007) Identification of a 150 bp cis-acting element of the AtNRT2. 1 promoter involved in the regulation of gene expression by the N and C status of the plant. Plant Cell Environ 30: 1366-1380.
52. Girin T, El-Kafafi E-S, Widiez T, Erban A, Hubberten HM, Kopka J, Hoefgen R, Gojon A, Lepetit M (2010) Identification of arabidopsis mutants impaired in the systemic regulation of root nitrate uptake by the nitrogen status of the plant. Plant Physiol 153: 1250-1260.
53. - uptake and reduction in Nicotiana plants. Plant Cell Environ 21: 43-53.
54. Gojon A, Nacry P, Davidian JC (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Curr Opin Plant Biol 12: 328-338.
55. Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J Exp Bot 62: 2299-2308.
56. Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Biotech 22: 245-252.
57. Gross M (2012) We need to talk about nitrogen. Curr Biol 22: R1-R4.
58. Hachiya T, Mizokami Y, Miyata K, Tholen D, Watanabe CK, Noguchi K (2011) Evidence for a nitrate-independent function of the nitrate sensor NRT1. 1 in Arabidopsis thaliana. J Plant Res 124: 425-430.
59. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14: 889-902.
60. Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11: 610-617.
61. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156: 1078-1086.
62. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
63. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol 139: 479-494.
64. Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22: 811-820.
65. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88: 150-164.
66. Hoque MS, Masle J, Udvardi MK, Ryan PR, Upadhyaya NM (2006) Over-expression of the rice OsAMT1-1 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammonium nutrition. Funct Plant Biol 33: 153-163.
67. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57: 264-278.
68. Huang NC, Chiang CS, Crawford NM, Tsay YF (1996) CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8: 2183-2191.
69. Huang NC, Liu KH, Lo HJ, Tsay YF (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11: 1381-1392.
70. Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105: 3-7.
71. Ishikawa S, Ito Y, Sato Y, Fukaya Y, Takahashi M, Morikawa H, Ohtake N, Ohyama T, Sueyoshi K (2009) Two-component high-affinity nitrate transport system in barley: membrane localization, protein expression in roots and a direct protein-protein interaction. Plant Biotechnol 26: 197-205.
72. Jackson WA, Volk RJ, Tucker TC (1972) Apparent induction of nitrate uptake in nitrate-depleted plants. Agron J 64: 518-528.
73. Jones DL, Shannon D, Junvee-Fortune T, Farrarc JF (2005) Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol Biochem 37: 179-181.
74. + transporter AtAMT1-1. Plant Physiol 130: 1263-1275.
75. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci U S A 109(24): 9653-9658.
76. Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7: e1002021.
77. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57: 313-321.
78. Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62: 1399-1409.
79. Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, Miller A, Daniel-Vedele F, Sakakibara H, Krapp A (2012) The Arabidopsis nitrate transporter NRT2. 4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24: 245-258.
80. King BJ, Siddiqi MY, Ruth TJ, Warner RL, Glass A (1993) Feedback regulation of nitrate influx in barley roots by nitrate, nitrite, and ammonium. Plant Physiol 102: 1279-1286.
81. Kojima S, Bohner A, Gassert B, Yuan L, von Wiren N (2007) AtDUR3 represents the major transporter for high-affinity urea transport across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 52: 30-40.
82. Kotur Z, Mackenzie N, Ramesh S, Tyerman SD, Kaiser BN, Glass ADM (2012) Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2. 1. New Phytol 194: 724-731.
83. Krapp A, Fraisier V, Scheible W-R, Quesada A, Gojon A, Stitt M, Caboche M, Daniel-Vedele F (1998) Expression studies of Nrt2;1 Np, a putative high-affinity nitrate transporter: evidence for its role in nitrate uptake. Plant J 14: 723-731.
84. -demand" signalling in Arabidopsis. Plant Physiol 142: 1075-1086.
85. Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010a) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13: 266-273.
86. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010b) Nitrate-regulated auxin transport by NRT1. 1 defines a mechanism for nutrient sensing in plants. Dev Cell 18: 927-937.
87. Krouk G, Ruffel S, Gutierrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16: 178-182.
88. + transporters in roots of Oryza sativa subspecies indica. Plant Cell Environ 26: 907-914.
89. Kumar A, Kaiser BN, Siddiqi MY, Glass ADM (2006) Functional characterization of OsAMT1. 1 overexpression lines of rice, Oryza sativa. Funct Plant Biol 33: 339-346.
90. Lainé P, Ourry A, Boucaud J (1995) Shoot control of nitrate uptake rates by roots of Brassica napus L.: effects of localized nitrate supply. Planta 196: 77-83.
91. Lanquar V, Loqué D, Hörmann F, Yuan L, Bohner A, Engelsberger WR, Lalonde S, Schulze WX, von Wirén N, Frommer WB (2009) Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis. Plant Cell 21: 3610-3622.
92. Laugier E, Bouguyon E, Mauriès A, Tillard P, Gojon A, Lejay L (2012) Regulation of high-affinity nitrate uptake in roots of Arabidopsis depends predominantly on posttranscriptional control of the NRT2. 1/NAR2. 1 transport system. Plant Physiol 158: 1067-1078.
93. Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB (1996) Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc Natl Acad Sci USA 93: 8139-8144.
94. Lee RB (1993) Control of net uptake of nutrients by regulation of influx in barley plants recovering from nutrient deficiency. Ann Bot 72: 223-230.
95. Lee YH, Foster J, Chen J, Voll LM, Weber AP, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50: 305-319.
96. Lehmann S, Gumy C, Blatter E, Boeffel S, Fricke W, Rentsch D (2011) In planta function of compatible solute transporters of the AtProT family. J Exp Bot 62: 787-796.
97. - uptake systems by N- and C-status of Arabidopsis plants. Plant J 18: 509-519.
98. Lesuffleur F, Paynel F, Bataille MP, Le Deunff E, Cliquet JB (2007) Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant Soil 294: 235-246.
99. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2. 1: AtNRT2. 2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143: 425-433.
100. Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1. 8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22: 1633-1646.
101. Lima JE, Kojima S, Takahashi H, von Wirén N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22: 3621-3633.
102. Lin CM, Koh S, Stacey G, Yu SM, Lin TY, Tsay YF (2000) Cloning and functional characterization of a constitutively expressed nitrate transporter gene, OsNRT1, from rice. Plant Physiol 122: 379-388.
103. 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: 751-760.
104. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22: 1005-1013.
105. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11: 865-874.
106. Liu L-H, Ludewig U, Frommer WB, von Wiren N (2003a) AtDUR3 encodes a new type of high affinity urea /H + symporter in Arabidopsis. Plant Cell 15: 790-800.
107. Liu L-H, Ludewig U, Gassert B, Frommer WB, von Wirén N (2003b) Urea transport by nitrogen-regulated tonoplast intrinsic TIP proteins in Arabidopsis. Plant Physiol 133: 1220-1228.
108. Liu TY, Chang CY, Chiou TJ (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12: 312-319.
109. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón 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: 244-256.
110. Loqué D, Yuan L, Kojima S, Gojon A, Wirth J, Gazzarrini S, Ishiyama K, Takahashi H, von Wiren N (2006) Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 48: 522-534.
111. Loqué D, Lalonde S, Looger LL, von Wiren N, Frommer WB (2007) A cytosolic trans-activation domain essential for ammonium uptake. Nature 446: 195-198.
112. Ludewig U, von Wiren N, Rentsch D, Frommer WB (2001) Rhesus factors and ammonium: a function in efflux? Genome Biol. 2, reviews 1010.
113. + by the root hair plasma membrane ammonium transporter LeAMT1-1. J Biol Chem 277: 13548-13555.
114. Ludewig U, Wilken S, Wu B, Jost W, Obrdlik P, El Bakkoury M, Marini AM, Andre B, Hamacher T, Boles E, von Wiren N, Frommer WB (2003) Homo- and hetero-oligomerization of ammonium transporter-1 NH4 uniporters. J Biol Chem 278: 45603-45610.
115. Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55(5): 493-512.
116. Lynch JP, Brown KM (2012) New roots for agriculture: exploiting the root phenome. Phylosophical Trans R Soc B-Biol Sci 367(1595): 1598-1604.
117. + uptake of Barley (Hordeum-Vulgare L) seedlings. J Plant Physiol 144: 351-357.
118. Malagoli P, Laine P, Le Deunff E, Rossato L, Ney B, Ourry A (2004) Modeling nitrogen uptake in oilseed rape cv Capitol during a growth cycle using influx kinetics of root nitrate transport systems and field experimental data. Plant Physiol 134: 388-400.
119. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London.
120. Merigout P, Lelandais M, Bitton F, Renou JP, Briand X, Meyer C, Daniel-Vedele F (2008) Physiological and transcriptomic aspects of urea uptake and assimilation in Arabidopsis plants. Plant Physiol 147: 1225-1238.
121. Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58: 2297-2306.
122. Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128-138.
123. Morere-Le Paven MC, Viau L, Hamon A, Vandecasteele C, Pellizzaro A, Bourdin C, Laffont C, Lapied B, Lepetit M, Frugier F, Legros C, Limami AM (2011) Characterization of a dual-affinity nitrate transporter MtNRT1. 3 in the model legume Medicago truncatula. J Exp Bot 62: 5595-5605.
124. - uptake by various phloem-translocated amino acids in soybean seedlings. J Exp Bot 43: 617-623.
125. Munos S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A (2004) Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1. 1 in the regulation of another nitrate transporter, NRT2. 1. Plant Cell 16: 2433-2447.
126. Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182: 31-48.
127. Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I, Tillard P, Zhuo D, Glass AD, Touraine B (2003) Regulation of the nitrate transporter gene AtNRT2. 1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol Biol 52: 689-703.
128. Nero D, Krouk G, Tranchina D, Coruzzi GM (2009) A system biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive "biomodule". BMC Syst Biol 3: 59.
129. + transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiol 143: 1651-1659.
130. + transporter from plants. EMBO J 13: 3464-3471.
131. Nobbe F (1862) Uber die feinere Verästelung der Pflanzenwurzeln. Landwirtschaftlichen Versuchs-Stationen 4: 212-224.
132. Ohlen E, Larsson CM (1992) Nitrate assimilatory properties of barley grown under long-term N-limitation: effects of local nitrate supply in split-root cultures. Physiol Plant 85: 9-16.
133. Ohlund J, Nasholm T (2001) Growth of conifer seedlings on organic and inorganic nitrogen sources. Tree Physiol 18: 1319-1326.
134. Okamoto M, Vidmar JJ, Glass AD (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44: 304-317.
135. Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass AD (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3. 1. Plant Physiol 140: 1036-1046.
136. Orsel M, Krapp A, Daniel-Vedele F (2002) Analysis of the NRT2 nitrate transporter family in Arabidopsis. Structure and gene expression. Plant Physiol 129: 886-896.
137. Orsel M, Chopin F, Leleu O, Smith SJ, Krapp A, Daniel-Vedele F, Miller AJ (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction. Plant Physiol 142: 1304-1317.
138. Pages L (2011) Links between root developmental traits and foraging performance. Plant Cell Environ 34(10): 1749-1760.
139. Palmer SJ, Berridge DM, McDonald AJS, Davies WJ (1996) Control of leaf expansion in sunflower (Helianthus annuus L.) by nitrogen nutrition. J Exp Bot 47: 359-368.
140. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53: 731-738.
141. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther DF, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150: 1541-1555.
142. Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and rye-grass. Plant Soil 229: 235-243.
143. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136: 2887-2894.
144. 2. Glob Chang Biol 12: 561-567.
145. Plett D, Toubia J, Garnett T, Tester M, Kaiser BN, Baumann U (2010) Dichotomy in the NRT gene families of dicots and grass species. PLoS One 5: e15289.
146. Poirier Y, Thoma S, Somerville C, Schiefelbein J (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97: 1087-1093.
147. Radin JW, Eidenbock MP (1986) Carbon accumulation during photosynthesis in leaves of nitrogen- and phosphorus-stressed cotton. Plant Physiol 82: 869-871.
148. - induced stimulation of leaf growth. J Exp Bot 56: 1143-1152.
149. + uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant J 19: 143-152.
150. Reinhold L, Kaplan A (1984) Membrane transport of sugars and amino acids. Ann Rev Plant Physiol 35: 45-83.
151. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1. 1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103: 19206-19211.
152. Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581: 2281-2289.
153. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127: 635-674.
154. Robinson D, Hodge A, Griffiths BS, Fitter AH (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc R Soc Lond B Biol 265: 431-435.
155. Rothstein SJ (2007) Returning to our roots: making plant biology research relevant to future challenges in agriculture. Plant Cell 19: 2695-2699.
156. 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 J 65: 557-570.
157. Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21(11): 3567-3584.
158. Rubio V, Bustos R, Irigoyen ML, Cardona-Lopez X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69: 361-373.
159. Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, van der Merwe MJ, Kakar K, Gouzy J, Fernie AR, Udvardi M, Salon C, Gojon A, Lepetit M (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146: 2020-2035.
160. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108: 18524-18529.
161. Rufty TW, Huber SC, Volk RJ (1988) Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol 88: 725-730.
162. 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: 337-344.
163. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11: 440-448.
164. Samuelson ME, Larsson CM (1993) Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium. Plant Sci 93: 77-84.
165. Santi S, Locci G, Monte R, Pinton R, Varanini Z (2003) Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase isoforms. J Exp Bot 54: 1851-1864.
166. Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K, Matsuoka K, Murata Y, Yamamoto Y (2010) Closing plant stomata requires a homologue of an aluminium-activated malate transporter. Plant Cell Physiol 51: 354-365.
167. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (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: 2483-2499.
168. + nitrogen in situ: plants compete well for amino acid N. Ecology 77: 2142-2147.
169. Schobert C, Komor E (1987) Amino acid uptake by Ricinus communis roots: characterization and physiological significance. Plant Cell Environ 10: 493-500.
170. Segonzac C, Boyer JC, Ipotesi E, Szponarski W, Tillard P, Touraine B, Sommerer N, Rossignol M, Gibrat R (2007) Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell 19: 3760-3777.
171. Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating them regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28: 655-662.
172. Sohlenkamp C, Shelden M, Howitt S, Udvardi M (2000) Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants. FEBS Lett 467: 273-278.
173. Sonoda Y, Ikeda A, Saiki S, von Wirén N, Yamaya T, Yamaguchi J (2003a) Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice. Plant Cell Physiol 44: 726-734.
174. Sonoda Y, Ikeda A, Saiki S, Yamaya T, Yamaguchi J (2003b) Feedback regulation of the ammonium transporter gene family AMT1 by glutamine in rice. Plant Cell Physiol 44: 1396-1402.
175. Stitt M (1999) Nitrate regulation of metabolism and growth. Cur Opin Plant Biol 2: 178-186.
176. Suenaga A, Moriya K, Sonoda Y, Ikeda A, Von Wirén N, Hayakawa T, Yamaguchi J, Yamaya T (2003) Constitutive expression of a novel-type ammonium transporter OsAMT2 in rice plants. Plant Cell Physiol 44: 206-211.
177. Svennerstam H, Ganeteg U, Bellini C, Näsholm T (2007) Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiol 143: 1853-1860.
178. Svennerstam H, Ganeteg U, Näsholm T (2008) Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. New Phytol 180: 620-630.
179. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39: 792-796.
180. Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42: 85-93.
181. Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45: 1053-1062.
182. 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: 259-262.
183. Tegeder M (2012) Transporters for amino acids in plant cells: some functions and many unknowns. Curr Opin Plant Biol 15(3): 315-321.
184. Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant Cell Environ 28: 813-821.
185. Tian QY, Chen FJ, Zhang FS, Mi GH (2005) Possible involvement of cytokinin in nitrate-mediated root growth in maize. Plant Soil 100: 1-12.
186. Tian Q, Chen F, Liu J, Zhang F, Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165: 942-951.
187. Tian QY, Sun P, Zhang W-H (2009) Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana. New Phytol 184: 918-931.
188. - uptake in Ricinus communis plants? J Exp Bot 49: 1371-1379.
189. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418: 671-677.
190. Tong Y, Zhou JJ, Li Z, Miller AJ (2005) A two-component high-affinity nitrate uptake system in barley. Plant J 41: 442-450.
191. - transporter? Plant Physiol 114: 137-144.
192. Trueman LJ, Richardson A, Forde BG (1996) Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 175: 223-231.
193. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72: 705-713.
194. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581: 2290-2300.
195. Tsay YF, Ho CH, Chen HY, Lin SH (2011) Integration of nitrogen and potassium signaling. Ann Rev Plant Biol 62: 207-226.
196. van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178: 185-192.
197. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutierrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 4477-4482.
198. Vidmar JJ, Zhuo D, Siddiqi MY, Schjoerring JK, Touraine B, Glass AD (2000) Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol 123: 307-318.
199. von Wirén N, Merrick M (2004) Regulation and function of ammonium carriers in bacteria, fungi and plants. Top Curr Genet 9: 95-120.
200. von Wirén N, Gazzarrini S, Gojon A, Frommer WB (2000a) The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 3: 254-261.
201. von Wirén N, Lauter F-R, Ninnemann O, Gillissen B, Walch-Liu P, Engels C, Jost W, Frommer WB (2000b) Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J 21: 167-175.
202. Wagner B, Beck E (1993) Cytokinins in the perennial herb Urtica dioica L. as influenced by its nitrogen status. Planta 190: 511-518.
203. Walch-Liu P, Forde BG (2008) Nitrate signalling mediated by the NRT1. 1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. Plant J 54: 820-828.
204. Walch-Liu P, Filleur S, Gan Y, Forde BG (2005) Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply. Photosynth Res 83: 239-250.
205. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97: 875-881.
206. Wang YY, Tsay YF (2011) Arabidopsis nitrate transporter NRT1. 9 is important in phloem nitrate transport. Plant Cell 23: 1945-1957.
207. +. Plant Physiol 103: 1249-1258.
208. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95: 15134-15139.
209. Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12: 1491-1510.
210. 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: 556-567.
211. Wang R, Tischner R, Gutierrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136: 2512-2522.
212. Wang W-H, Köhler B, Cao F-Q, Liu L-H (2008) Molecular and physiological aspects of urea transport in higher plants. Plant Sci 175: 467-477.
213. Wang R, Xing X, Wang Y, Tran A, Crawford NM (2009) A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1. 1. Plant Physiol 151: 472-478.
214. Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8): 458-467.
215. West CE, Waterworth WM, Stephens SM, Smith CP, Bray CM (1998) Cloning and functional characterization of a peptide transporter expressed in the scutellum of barley. Plant J 15: 221-229.
216. - uptake is associated with changes in histone methylation. Proc Natl Acad Sci USA 108: 13329-13334.
217. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126.
218. Wirth J, Chopin F, Santoni V, Viennois G, Tillard P, Krapp A, Lejay L, Daniel-Vedele F, Gojon A (2007) Regulation of root nitrate uptake at the NRT2. 1 protein level in Arabidopsis thaliana. J Biol Chem 282: 23541-23552.
219. Witte C-P (2011) Urea metabolism in plants. Plant Sci 180: 431-438.
220. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63: 153-182.
221. Yendrek CR, Lee YC, Morris V, Liang Y, Pislariu CI, Burkart G, Meckfessel MH, Salehin M, Kessler H, Wessler H, Lloyd M, Lutton H, Teillet A, Sherrier DJ, Journet EP, Harris JM, Dickstein R (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J 62: 100-112.
222. Yoh SM, Lucas JS, Jones KA (2008) The Iws1: Spt6: CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev 22: 3422-3434.
223. Yong Z, Kotur Z, Glass AD (2010) Characterization of an intact two-component high-affinity nitrate transporter from Arabidopsis roots. Plant J 63: 739-748.
224. Yuan L, Loqué D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wiren N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19: 2636-2652.
225. Yuan L, Graff L, Loqué D, Kojima S, Tsuchiya YN, Takahashi H, von Wirén N (2009) AtAMT1;4, a pollen-specific high-affinity ammonium transporter of the plasma membrane in Arabidopsis. Plant Cell Physiol 50: 13-25.
226. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409.
227. Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51: 51-59.
228. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96: 6529-6534.
229. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58: 2329-2338.
230. Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190: 906-915.
231. Zhou JJ, Fernandez E, Galvan A, Miller AJ (2000) A high affinity nitrate transport system from Chlamydomonas requires two gene products. FEBS Lett 466: 225-227.
232. Zhuo D, Okamoto M, Vidmar JJ, Glass AD (1999) Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J 17: 563-568.