Local and long-range signaling pathways regulating plant responses to nitrate

Annual Review of Plant Biology

Volumn 53, Issue , 2002, Pages 203-224

  Forde, Brian G ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Auxin; Cytokinin; Lateral roots; Leaf expansion; Nitrate transport

Indexed keywords

NITRATE;

GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

NITRATES; PLANT PHYSIOLOGY; PLANTS; SIGNAL TRANSDUCTION;

EID: 0036999943     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.53.100301.135256     Document Type: Review

References (141)

1. Ballaré CL. 1999. Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. Trends Plant Sci. 4:97-102
2. Beck EH. 1996. Regulation of shoot/root ratio by cytokinins from roots in Urtica dioica: opinion. Plant Soil 185:3-12
3. Beligni MV, Lamattina L. 2001. Nitric oxide in plants: the history is just beginning. Plant Cell Environ. 24:267-78
4. Berleth T, Sachs T. 2001. Plant morphogenesis: long-distance coordination and local patterning. Curr. Opin. Plant Biol. 4:57-62
5. Bingham IJ, Blackwood JM, Stevenson EA. 1998. Relationship between tissue sugar content, phloem import and lateral root initiation in wheat. Physiol. Plant 103:107-13
6. Bloom AJ. 1997. Interactions between inorganic nitrogen nutrition and root development. Z. Pflanz. Bodenk. 160:253-59
7. Brandstatter I, Kieber JJ. 1998. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell 10:1009-19
8. 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
9. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, et al. 2001. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843-52
10. Celenza JL, Grisafi PL, Fink GR. 1995. A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 9:2131-42
11. --uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol. 127:262-71
12. Chang C, Stadler R. 2001. Ethylene hormone receptor action in Arabidopsis. BioEssays 23:619-27
13. 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. 40:753-62
14. Coruzzi G, Bush DR. 2001. Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol. 125:61-64
15. Coruzzi GM, Zhou L. 2001. Carbon and nitrogen sensing and signaling in plants: emerging "matrix effects." Curr. Opin. Plant Biol. 4:247-53
16. Crawford NM. 1995. Nitrate: nutrient and signal for plant growth. Plant Cell 7:859-68
17. Crawford NM, Arst HN. 1993. The molecular genetics of nitrate assimilation in fungi and plants. Annu. Rev. Genet. 27:115-46
18. Crawford NM, Forde BG. 2002. Molecular and developmental biology of inorganic nitrogen nutrition. In The Arabidopsis Book, ed. E Meyerowitz, C Somerville. In press (online ref.)
19. Crawford NM, Guo F-Q. 2002. Regulation of the dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) during vegetative and reproductive development in Arabidopsis. J. Exp. Bot. In press
20. 2 on the developmental physiology of roots: the use of Arabidopsis thaliana. J. Exp. Bot. 49:593-97
21. D'Agostino IB, Deruere J, Kieber JJ. 2000. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124:1706-17
22. D'Agostino IB, Kieber JJ. 1999. Molecular mechanisms of cytokinin action. Curr. Opin. Plant Biol. 2:359-64
23. Daniel-Vedele F, Filleur S, Caboche M. 1998. Nitrate transport: a key step in nitrate assimilation. Curr. Opin. Plant Biol. 1:235-39
24. --influx, efflux, and N utilization in the plant during the day-night cycle. J. Exp. Bot. 46:1585-94
25. Deng MD, Moureaux T, Caboche M. 1989. Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol. 91:304-9
26. De Veylder L, Engler JD, Burssens S, Manevski A, Lescure B, et al. 1999. A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208:453-62
27. Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75:479-90
28. Drew MC, Saker LR. 1975. Nutrient supply and the growth of the seminal root system of barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J. Exp. Bot. 26:79-90
29. Drew MC, Saker LR, Ashley TW. 1973. Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. J. Exp. Bot. 24:1189-202
30. Ericsson T. 1995. Growth and shoot: root ratio of seedlings in relation to nutrient availability. Plant Soil 168-69:205-14
31. Farrar J. 1996. Regulation of root weight ratio is mediated by sucrose: opinion. Plant Soil 185:13-19
32. Filleur S, Daniel-Vedele F. 1999. Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207:461-69
33. Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F, et al. 2001. An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett. 489:220-24
34. Forde BG. 2000. Nitrate transporters in plants: structure, function and regulation. Biochim. Biophys. Acta 1465:219-35
35. Forde BG, Clarkson DT. 1999. Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Adv. Bot. Res. 30:1-90
36. Forde BG, Lorenzo H. 2001. The nutritional control of root development. Plant Soil 232:51-68
37. 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. 23:489-96
38. Friend AL, Eide MR, Hinckley TM. 1990. Nitrogen stress alters root proliferation in Douglas fir seedlings. Can. J. For. Res. 20:1524-29
39. Galván A, Fernández E. 2001. Eukaryotic nitrate and nitrite transporters. Cell. Mol. Life Sci. 58:225-33
40. +-transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. Plant J. 26:143-55
41. Genoud T, Métraux J-P. 1999. Crosstalk in plant cell signaling: structure and function of the genetic network. Trends Plant Sci. 4:503-7
42. Gibson SI. 2000. Plant sugar-response pathways. Part of a complex regulatory web. Plant Physiol. 124:1532-39
43. Glass ADM, Brito DT, Kaiser BN, Kronzucker HJ, Kumar A, et al. 2001. Nitrogen transport in plants, with an emphasis on the regulation of fluxes to match plant demand. Z. Pflanz. Bodenk. 164:199-207
44. -- uptake and reduction in Nicotiana plants. Plant Cell Environ. 21:43-53
45. Gowri G, Kenis JD, Ingemarsson B, Redinbaugh MG, Campbell WH. 1992. Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol. Biol. 18:55-64
46. Guo F-Q, Wang RC, Chen M, Crawford NM. 2001. The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13:1-18
47. Hobbie L, Estelle M. 1995. The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J. 7:211-20
48. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 1999. Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biol. Biochem. 31:1517-30
49. Hsieh M-H, Lam H-M, 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
50. Hutchings MJ, de Kroon H. 1994. Foraging in plants: the role of morphological plasticity in resource acquisition. Adv. Ecol. Res. 25:159-238
51. Hwang CF, Lin Y, Dsouza T, Cheng CL. 1997. Sequences necessary for nitrate-dependent transcription of Arabidopsis nitrate reductase genes. Plant Physiol. 113:853-62
52. Imsande J, Touraine B. 1994. N demand and the regulation of nitrate uptake. Plant Physiol. 105:3-7
53. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, et al. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060-63
54. Kakimoto T. 1996. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982-85
55. Krapp A, Fraisier V, Scheible WR, Quesada A, Gojon A, et al. 1998. Expression studies of Nrt2:1Np, a putative high-affinity nitrate transporter: evidence for its role in nitrate uptake. Plant J. 14:723-31
56. Kunze M, Riedel J, Lange U, Hurwitz R, Tischner R. 1997. Evidence for the presence of GPI-anchored PM-NR in leaves of Beta vulgaris and for PM-NR in barley leaves. Plant Physiol. Biochem 35:507-12
57. 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
58. --uptake rate and growth of roots in Lolium multiflorum Lam. Plant Soil 202:61-67
59. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM. 1996. The molecular genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:569-93
60. Lebot J, Kirkby EA. 1992. Diurnal uptake of nitrate and potassium during the vegetative growth of tomato plants. J. Plant Nutr. 15:247-64
61. --uptake systems by N- and C-status of Arabidopsis plants. Plant J. 18:509-19
62. Leydecker MT, Camus I, Daniel-Vedele F, Truong HN. 2000. Screening for Arabidopsis mutants affected in the Nii gene expression using the GUS reporter gene. Physiol. Plant. 108:161-70
63. Leyser O, Fitter A. 1998. Roots are branching out in patches. Trends Plant Sci. 3:203-4
64. Lorenz MC, Heitman J. 1998. The MEP2 ammonium permease regulates pseudohyphal differentiaition in Saccharomyces cerevisiae. EMBO J. 17:1236-47
65. MacKintosh C, Meek SEM. 2001. Regulation of plant NR activity by reversible phosphorylation, 14-3-3 proteins and proteolysis. Cell. Mol. Life Sci. 58:205-14
66. Marschner H. 1995. Mineral Nutrition of Higher Plants. London: Academic. 889 pp.
67. Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M. 2001. The immediate cause of the diurnal changes of nitrogen metabolism in leaves of nitrate-replete tobacco: a major imbalance between the rate of nitrate reduction and the rates of nitrate uptake and ammonium metabolism during the first part of the light period. Plant Cell Environ. 24:177-90
68. McDonald AJS, Davies WJ. 1996. Keeping in touch: responses of the whole plant to deficits in water and nitrogen supply. Adv. Bot. Res. 22:229-300
69. Meyer C, Stitt M. 2001. Nitrate reduction and signalling. In Plant Nitrogen, ed. PJ Lea, J-F Morot-Gaudry, pp. 37-59. Heidelberg: Springer
70. --uptake in Ricinus communis. Plant Soil 226:87-98
71. Mockaitis K, Howell SH. 2000. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J. 24:785-96
72. Mok DWS, Mok MC. 2001. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:89-118
73. Neininger A, Back E, Bichler J, Schneiderbauer A, Mohr H. 1994. Deletion analysis of a nitrite reductase promoter from spinach in transgenic tobacco. Planta 194:186-92
74. Ninfa AJ, Atkinson MR. 2000. PII signal transduction proteins. Trends Microbiol. 8:172-79
75. 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
76. Ono F, Frommer WB, von Wiren N. 2000. Coordinated diurnal regulation of low- and high-affinity nitrate transporters in tomato. Plant Biol. 2:17-23
77. Orsel M, Filleur S, Fraisier V, Daniel-Vedele F. 2002. Nitrate transport in plants: which gene and which control? J. Exp. Bot. In press
78. Padgett PE, Leonard RT. 1996. Free amino acid levels and the regulation of nitrate uptake in maize cell suspension cultures. J. Exp. Bot. 47:871-83
79. Pearson CJ, Steer BT. 1977. Daily changes in nitrate uptake and metabolism in Capsicum annuum. Planta 137:107-12
80. Peuke AD, Hartung W, Jeschke WD. 1994. The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. II. Grown with low or high nitrate supply. J. Exp. Bot. 45:733-40
81. Pouteau S, Cherel I, Vaucheret H, Caboche M. 1989. Nitrate reductase mRNA regulation in Nicotiana plumbaginifolia nitrate reductase-deficient mutants. Plant Cell 1:1111-20
82. Prosser IM, Purves JV, Saker LR, Clarkson DT. 2001. Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. J. Exp. Bot. 52:113-21
83. Rastogi R, Bate NJ, Sivasankar S, Rothstein SJ. 1997. Footprinting of the spinach nitrite reductase gene promoter reveals the preservation of nitrate regulatory elements between fungi and higher plants. Plant Mol. Biol. 34:465-76
84. Redinbaugh MG, Campbell WH. 1991. Higher plant responses to environmental nitrate. Physiol. Plant 82:640-50
85. Redinbaugh MG, Campbell WH. 1993. Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root primary response to nitrate: evidence for an organ-specific response. Plant Physiol. 101:1249-55
86. Reed RC, Brady SR, Muday GK. 1998. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in arabidopsis. Plant Physiol. 118:1369-78
87. Reisenauer HM. 1966. Mineral nutrients in soil solution. In Environmental Biology, ed. PL Altman, DS Dittmer, pp. 507-8, Bethesda, MA: Fed. Am. Soc. Exp. Biol.
88. Robinson D. 1994. The responses of plants to non-uniform supplies of nutrients. New Phytol. 127:635-74
89. Robinson D. 2001. Root proliferation, nitrate inflow and their carbon costs during nitrogen capture by competing plants in patchy soil. Plant Soil 232:41-50
90. Robinson D, Hodge A, Griffiths BS, Fitter AH. 1999. Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc. R. Soc. Lond. Ser. B 266:431-35
91. Roggatz U, McDonald AJS, Stadenberg I, Schurr U. 1999. Effects of nitrogen deprivation on cell division and expansion in leaves of Ricinus communis L. Plant Cell Environ. 22:81-89
92. --transport. Plant Cell Physiol. 37:285-91
93. Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M. 1998. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev. 12:198-207
94. --influx in phosphorus-limited plants. Plant Sci. 76:43-48
95. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ. 2001. The phloem as a conduit for inter-organ communication. Curr. Opin. Plant Biol. 4:202-9
96. Sablowski RWM, Meyerowitz EM. 1998. A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93-103
97. Sakakibara H, Kobayashi K, Deji A, Sugiyama T. 1997. Partial characterization of the signaling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leaves. Plant Cell Physiol. 38:837-43
98. 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
99. Sakakibara H, Taniguchi M, Sugiyama T. 2000. His-Asp phosphorelay signaling: a communication avenue between plants and their environment. Plant Mol. Biol. 42:273-78
100. 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
101. Sattelmacher B, Marschner H. 1978. Nitrogen nutrition and cytokinin activity in Solanum tuberosum. Physiol. Plant 42:185-89
102. 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
103. Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M. 1997. Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J. 11:671-91
104. Shen WH. 2001. The plant cell cycle: G1/S regulation. Euphytica 118:223-32
105. Shiraishi N, Imanishi M, Endo T, Sugimoto T, Oji Y. 2001. Investigation of transcription factor of spinach nitrate reductase. Presented at Int. Symp. Inorg. N Assim., 6th, Reims
106. Sivasankar S, Rastogi R, Jackman L, Oaks A, Rothstein S. 1998. Analysis of cis-acting DNA elements mediating induction and repression of the spinach nitrite reductase gene. Planta 206:66-71
107. Smeekens S. 2000. Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:49-81
108. Stewart V. 1994. Regulation of nitrate and nitrite reductase synthesis in enterobacteria. Ant. Van Leeuw. Int. J. Gen. Mol. Microbiol. 66:37-45
109. Stitt M. 1999. Nitrate regulation of metabolism and growth. Curr. Opin. Plant Biol. 2:178-86
110. Stitt M, Feil R. 1999. Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root. Plant Soil 215:143-53
111. Stitt M, Krapp A. 1999. The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ. 22:583-621
112. Stöhr C, Schuler F, Tischner R. 1995. Glycosyl-phosphatidylinositol-anchored proteins exist in the plasma membrane of Chlorella saccharophila (Kruger) Nadson: plasma membrane-bound nitrate reductase as an example. Planta 196:284-87
113. Stöhr C, Strube F, Marx G, Ullrich WR, Rockel P. 2001. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212:835-41
114. Sueyoshi K, Kleinhofs A, Warner RL. 1995. Expression of NADH-specific and NAD(P)H-bispecific nitrate reductase genes in response to nitrate in barley. Plant Physiol. 107:1303-11
115. Sueyoshi K, Mitsuyama T, Sugimoto T, Kleinhofs A, Warner RL, Oji Y. 1999. Effects of inhibitors for signaling components on the expression of the genes for nitrate reductase and nitrite reductase in excised barley leaves. Soil Sci. Plant Nutr. 45:1015-19
116. Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, Mizuno T. 2001. The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol. 42:107-13
117. 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
118. 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
119. Thompson GA, Schulz A. 1999. Macromolecular trafficking in the phloem. Trends Plant Sci. 4:354-60
120. Tian Q, Reed JW. 1999. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711-21
121. --uptake in Ricinus communis plants? J. Exp. Bot. 49:1371-79
122. Tischner R. 2000. Nitrate uptake and reduction in higher and lower plants. Plant Cell Environ. 23:1005-24
123. Touraine B, Clarkson DT, Muller B. 1994. Regulation of nitrate uptake at the whole plant level. In A Whole Plant Perspective on Carbon-Nitrogen Interactions, ed. J Roy, E Garnier, pp. 11-30. Den Haag, The Neth.: SPB Acad. Publ.
124. Trewavas AJ. 1983. Nitrate as a plant hormone. In British Plant Growth Regulator Group Monograph 9, ed. MB Jackson, pp. 97-110. Oxford, UK: Br. Plant Growth Regul. Group
125. Urao T, Miyata S, Yamaguchi-Shinozaki K, Shinozaki K. 2000. Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett. 478:227-32
126. Urao T, Yamaguchi-Shinozaki K, Shinozaki K. 2000. Two-component systems in plant signal transduction. Trends Plant Sci. 5:67-74
127. van der Leij M, Smith SJ, Miller AJ. 1998. Remobilisation of vacuolar stored nitrate in barley root cells. Planta 205:64-72
128. Vidmar JJ, Zhuo D, Siddiqi MY, Schjoerring JK, Touraine B, Glass ADM. 2000. Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol. 123:307-18
129. Vidmar JJ, Zhuo DG, Siddiqi MY, Glass ADM. 2000. Isolation and characterization of HvNRT2.3 and HvNRT2.4, cDNAs encoding high-affinity nitrate transporters from roots of barley. Plant Physiol. 122:783-92
130. Walch-Liu P, Neumann G, Bangerth F, Engels C. 2000. Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J. Exp. Bot. 51:227-37
131. Walch-Liu P, Neumann G, Engels C. 2001. Response of shoot and root growth to supply of different nitrogen forms is not related to carbohydrate and nitrogen status of tobacco plants. Z. Pflanz. Bodenk. 164:97-103
132. Wang RC, 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 12:1491-509
133. Wang RC, Liu D, Crawford NM. 1998. The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl. Acad. Sci. USA 95:15134-39
134. Ward MR, Tischner R, Huffaker RC. 1988. Inhibition of nitrate transport by anti-nitrate reductase IgG fragments and the identification of plasma-membrane associated nitrate reductase in roots of barley seedlings. Plant Physiol. 88:1141-45
135. Warning HO, Hachtel W. 2000. Functional analysis of a nitrite reductase promoter from birch in transgenic tobacco. Plant Sci. 155:141-51
136. Xie Q, Frugis G, Colgan D, Chua NH. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14:3024-36
137. 5 reductase family, is required for entry into the phloem translocation pathway. Plant J. 24:735-47
138. Zhang HM, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407-9
139. Zhang HM, Forde BG. 2000. Regulation of Arabidopsis root development by nitrate availability. J. Exp. Bot. 51:51-59
140. Zhang HM, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. USA 96:6529-34
141. Zhuo D, Okamoto M, Vidmar JJ, Glass ADM. 1999. Regulation of a putative high-affinity nitrate transporter (NRT2; 1At) in roots of Arabidopsis thaliana. Plant J. 17:563-68