Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency

Journal of Experimental Botany

Volumn 62, Issue 4, 2011, Pages 1499-1509

  Kant, Surya ^a   Bi, Yong Mei ^a   Rothstein, Steven J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Assimilation; genetic improvement; nitrogen limitation; nitrogen use efficiency; remobilization

Indexed keywords

FERTILIZER; NITROGEN;

ADAPTATION; BREEDING; CHEMISTRY; CROP; ENVIRONMENT; GENE EXPRESSION PROFILING; GENETIC ENGINEERING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT; PLANT GENE; PLANT ROOT; REVIEW;

ADAPTATION, PHYSIOLOGICAL; BREEDING; CROPS, AGRICULTURAL; ENVIRONMENT; FERTILIZERS; GENE EXPRESSION PROFILING; GENES, PLANT; GENETIC ENGINEERING; NITROGEN; PLANT ROOTS; PLANTS;

EID: 79551712750     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq297     Document Type: Review

References (108)

1. Adam Z, Adamska I, Nakabayashi K, et al. 2001. Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclat (Pubitemid 32375773)
2. Anbessa Y, Juskiw P, Good A, Nyachiro J, Helm J. 2009. Genetic variability in nitrogen use efficiency of spring barley. Crop Science 49, 1259-1269.
3. Back E, Dunne W, Schneiderbauer A, Deframond A, Rastogi R, Rothstein SJ. 1991. Isolation of the spinach nitrite reductase gene promoter which confers nitrate inducibility on gus gene-expression in transgenic tobacco. Plant Molecular Biology 17, 9-18.
4. Bi YM, Kant S, Clark J, et al. 2009. Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant, Cell and Environment 32, 1749-1760.
5. Bi YM, Wang RL, Zhu T, Rothstein SJ. 2007. Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8, 281.
6. Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S. 2005. Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. The Plant Journal 44, 680-692.
7. Cabrera-Bosquet L, Molero G, Bort J, Nogues S, Araus JL. 2007. The combined effect of constant water deficit and nitrogen supply on WUE, NUE and Delta C-13 in durum wheat potted plants. Annals of Applied Biology 151, 277-289. (Pubitemid 350182350)
8. Caddick MX, Arst HN, Taylor LH, Johnson RI, Brownlee AG. 1986. Cloning of the regulatory gene area mediating nitrogen metabolite repression in Aspergillus nidulans. EMBO Journal 5, 1087-1090.
9. Castaings L, Camargo A, Pocholle D, et al. 2009. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant Journal 57, 426-435.
10. Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70, 1-9. (Pubitemid 129572610)
11. Chen LS, Ortiz-Lopez A, Jung A, Bush DR. 2001. ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiology 125, 1813-1820. (Pubitemid 32375764)
12. Crawford NM, Forde BG. 2002. Molecular and developmental biology of inorganic nitrogen nutrition. In: Meyerowitz EM, ed. The Arabidopsis book. Rockville, MD: American Society of Plant Biologists.
13. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H. 2006. The nitrate/ proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939-942. (Pubitemid 44285951)
14. Diaz C, Saliba-Colombani V, Loudet O, Belluomo P, Moreau L, Daniel-Vedele F, Morot-Gaudry JF, Masclaux-Daubresse C. 2006. Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant and Cell Physiology 47, 74-83. (Pubitemid 43278249)
15. Ding L, Wang KJ, Jiang GM, Biswas DK, Xu H, Li LF, Li YH. 2005. Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Annals of Botany 96, 925-930. (Pubitemid 41330561)
16. Firbank LG. 2005. Striking a new balance between agricultural production and biodiversity. Annals of Applied Biology 146, 163-175. (Pubitemid 40473874)
17. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD. 2008. Cell-specific nitrogen responses mediate developmental plasticity. Proceedings of the National Academy of Sciences, USA 105, 803-808. (Pubitemid 351171790)
18. Girin T, El-Kafafi el 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 Physiology 153, 1250-1260.
19. 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 and Environment 30, 1366-1380. (Pubitemid 47493859)
20. Glass ADM. 2003. Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Critical Reviews in Plant Sciences 22, 453-470.
21. Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C. 2010. Food security: the challenge of feeding 9 billion people. Science 327, 812-818.
22. 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. The Plant Cell 17, 3500-3512.
23. Good AG, Shrawat AK, Muench DG. 2004. Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends in Plant Science 9, 597-605. (Pubitemid 39558557)
24. Gutierrez RA, Gifford ML, Poultney C, Wang RC, Shasha DE, Coruzzi GM, Crawford NM. 2007a. Insights into the genomic nitrate response using genetics and the Sungear Software System. Journal of Experimental Botany 58, 2359-2367. (Pubitemid 47216544)
25. Gutierrez RA, Lejay LV, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM. 2007b. Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biology 8, R7.
26. Gutierrez RA, Stokes TL, Thum K, et al. 2008. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proceedings of the National Academy of Sciences, USA 105, 4939-4944. (Pubitemid 351753850)
27. Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA. 2001. The role of cytosolic glutamine synthetase in wheat. Annals of Applied Biology 138, 83-89. (Pubitemid 32623672)
28. +/amino acid permease gene expression during seed development of Arabidopsis. The Plant Journal 14, 535-544.
29. Ho CH, Lin SH, Hu HC, Tsay YF. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
30. Hofman-Bang J. 1999. Nitrogen catabolite repression in Saccharomyces cerevisiae. Molecular Biotechnology 12, 35-73. (Pubitemid 29530084)
31. Hu HC, Wang YY, Tsay YF. 2009. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. The Plant Journal 57, 264-278.
32. Inan G, Zhang Q, Li PH, et al. 2004. Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiology 135, 1718-1737. (Pubitemid 39009415)
33. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T. 2008. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiology 148, 142-155. (Pubitemid 352847588)
34. Jarai G, Truong HN, Danielvedele F, Marzluf GA. 1992. Nit2, the nitrogen regulatory protein of Neurospora crassa, binds upstream of Nia, the tomato nitrate reductase gene. in vitro. Current Genetics 21, 37-41.
35. Johnson DA, Hill JP, Thomas MA. 2006. The monosaccharide transporter gene family in land plants is ancient and shows differential subfamily expression and expansion across lineages. BMC Evolutionary Biology 6, .
36. Kant S, Bi YM, Weretilnyk E, Barak S, Rothstein SJ. 2008. The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogen-limiting conditions by maintaining growth, nitrogen uptake, and assimilation. Plant Physiology 147, 1168-1180. (Pubitemid 352844276)
37. + uptake in T. halophila. Plant, Cell and Environment 29, 1220-1234. (Pubitemid 43855740)
38. Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F. 2004. The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220, 97-104. (Pubitemid 40033004)
39. Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J. 2007. In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crops Research 102, 22-32. (Pubitemid 46613937)
40. Kichey T, Le Gouis J, Sangwan B, Hirel B, Dubois F. 2005. Changes in the cellular and subcellular localization of glutamine synthetase and glutamate dehydrogenase during flag leaf senescence in wheat (Triticum aestivum L.). Plant and Cell Physiology 46, 964-974. (Pubitemid 41435484)
41. Krouk G, Tranchina D, Lejay L, Cruikshank AA, Shasha D, Coruzzi GM, Gutierrez RA. 2009. A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PloS Computational Biology 5, .
42. Le Gouis J, Beghin D, Heumez E, Pluchard P. 2000. Genetic differences for nitrogen uptake and nitrogen utilisation efficiencies in winter wheat. European Journal of Agronomy 12, 163-173. (Pubitemid 30397760)
43. Lea PJ, Azevedo RA. 2007. Nitrogen use efficiency. 2. Amino acid metabolism. Annals of Applied Biology 151, 269-275. (Pubitemid 350178783)
44. Lian X, Wang S, Zhang J, Feng Q, Zhang L, Fan D, Li X, Yuan D, Han B, Zhang Q. 2006. Expression profiles of 10 422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Molecular Biology 60, 617-631. (Pubitemid 43673619)
45. Lin Y, Hwang CF, Brown JB, Cheng CL. 1994. 5' Proximal regions of Arabidopsis nitrate reductase genes direct nitrate-induced transcription in transgenic tobacco. Plant Physiology 106, 477-484.
46. Little DY, Rao HY, 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. Proceedings of the National Academy of Sciences, USA 102, 13693-13698. (Pubitemid 41420910)
47. Liu J, Wu YH, Yan JJ, Liu YD, Shen FF. 2008. Protein degradation and nitrogen remobilization during leaf senescence. Journal of Plant Biology 51, 11-19. (Pubitemid 351251438)
48. Liu X, Bush DR. 2006. Expression and transcriptional regulation of amino acid transporters in plants. Amino Acids 30, 113-120.
49. Lowry JA, Atchley WR. 2000. Molecular evolution of the GATA family of transcription factors: conservation within the DNA-binding domain. Journal of Molecular Evolution 50, 103-115. (Pubitemid 30429986)
50. Mae T, Thomas H, Gay AP, Makino A, Hidema J. 1993. Leaf development in Lolium temulentum: photosynthesis and photosynthetic proteins in leaves senescing under different irradiances. Plant and Cell Physiology 34, 391-399.
51. Malamy JE. 2005. Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell and Environment 28, 67-77. (Pubitemid 40141467)
52. Malamy JE, Ryan KS. 2001. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiology 127, 899-909. (Pubitemid 33112151)
53. Martin A, Lee J, Kichey T, et al. 2006. Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. The Plant Cell 18, 3252-3274. (Pubitemid 46013289)
54. Martin T, Oswald O, Graham IA. 2002. Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: nitrogen availability. Plant Physiology 128, 472-481. (Pubitemid 34190862)
55. Miller AJ, Fan XR, Orsel M, Smith SJ, Wells DM. 2007. Nitrate transport and signalling. Journal of Experimental Botany 58, 2297-2306. (Pubitemid 47216543)
56. Muchow RC. 1998. Nitrogen utilization efficiency in maize and grain sorghum. Field Crops Research 56, 209-216. (Pubitemid 28278294)
57. Naito T, Kiba T, Koizumi N, Yamashino T, Mizuno T. 2007. Characterization of a unique GATA family gene that responds to both light and cytokinin in Arabidopsis thaliana. Bioscience Biotechnology and Biochemistry 71, 1557-1560. (Pubitemid 47012022)
58. Namai S, Toriyama K, Fukuta Y. 2009. Genetic variations in dry matter production and physiological nitrogen use efficiency in rice (Oryza sativa L.) varieties. Breeding Science 59, 269-276.
59. Nero D, Krouk G, Tranchina D, Coruzzi GM. 2009. A systems biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive 'biomodule'. BMC Systems Biology 3.
60. O'Neill PM, Shanahan JF, Schepers JS, Caldwell B. 2004. Agronomic responses of corn hybrids from different eras to deficit and adequate levels of water and nitrogen. Agronomy Journal 96, 1660-1667. (Pubitemid 39588539)
61. Obara M, Sato T, Sasaki S, Kashiba K, Nagano A, Nakamura I, Ebitani T, Yano M, Yamaya T. 2004. Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice. Theoretical and Applied Genetics 110, 1-11. (Pubitemid 40240633)
62. Okumoto S, Koch W, Tegeder M, Fischer WN, Biehl A, Leister D, Stierhof YD, Frommer WB. 2004. Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. Journal of Experimental Botany 55, 2155-2168. (Pubitemid 39342618)
63. Oliveira IC, Coruzzi GM. 1999. Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis. Plant Physiology 121, 301-310.
64. Ono K, Terashima I, Watanabe A. 1996. Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant and Cell Physiology 37, 1083-1089. (Pubitemid 27141055)
65. OrtizMonasterio JI, Sayre KD, Rajaram S, McMahon M. 1997. Genetic progress in wheat yield and nitrogen use efficiency under four nitrogen rates. Crop Science 37, 898-904. (Pubitemid 27253303)
66. 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)-signalling hypothesis in plants. Genome Biology 5, R91.
67. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR. 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150, 1541-1555.
68. Paul MJ, Driscoll SP. 1997. Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. Plant, Cell and Environment 20, 110-116. (Pubitemid 27103334)
69. Peng M, Hudson D, Schofield A, Tsao R, Yang R, Gu H, Bi YM, Rothstein SJ. 2008. Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. Journal of Experimental Botany 59, 2933-2944.
70. Peng MS, Bi YM, Zhu T, Rothstein SJ. 2007a. Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Molecular Biology 65, 775-797. (Pubitemid 350159805)
71. Peng MS, Hannam C, Gu HL, Bi YM, Rothstein SJ. 2007b. A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. The Plant Journal 50, 320-337. (Pubitemid 46624139)
72. Presterl T, Seitz G, Landbeck M, Thiemt EM, Schmidt W, Geiger HH. 2003. Improving nitrogen-use efficiency in European maize: Estimation of quantitative genetic parameters. Crop Science 43, 1259-1265. (Pubitemid 36774853)
73. Price J, Laxmi A, St Martin SK, Jang JC. 2004. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. The Plant Cell 16, 2128-2150. (Pubitemid 39059733)
74. Rastogi R, Back E, Schneiderbauer A, Bowsher CG, Moffatt B, Rothstein SJ. 1993. A 330 bp region of the spinach nitrite reductase gene promoter directs nitrate-inducible tissue-specific expression in transgenic tobacco. The Plant Journal 4, 317-326.
75. 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 Molecular Biology 34, 465-476. (Pubitemid 27284880)
76. Raun WR, Johnson GV. 1999. Improving nitrogen use efficiency for cereal production. Agronomy Journal 91, 357-363. (Pubitemid 29402893)
77. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A. 2006a. The Arabidopsis NRT1.1 transporter participates in the signalling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences, USA 103, 19206-19211. (Pubitemid 350002851)
78. Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A. 2006b. 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 Physiology 140, 909-921. (Pubitemid 43956245)
79. Rentsch D, Hirner B, Schmelzer E, Frommer WB. 1996. Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. The Plant Cell 8, 1437-1446. (Pubitemid 26351949)
80. Reyes JC, Muro-Pastor MI, Florencio FJ. 2004. The GATA family of transcription factors in Arabidopsis and rice. Plant Physiology 134, 1718-1732. (Pubitemid 38527379)
81. Rothstein SJ. 2007. Returning to our roots: making plant biology research relevant to future challenges in agriculture. The Plant Cell 19, 2695-2699. (Pubitemid 350046221)
82. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor involved in phosphate starvation signalling both in vascular plants and in unicellular algae. Genes and Development 15, 2122-2133. (Pubitemid 32762055)
83. Rueda-Lopez M, Crespillo R, Canovas FM, Avila C. 2008. Differential regulation of two glutamine synthetase genes by a single Dof transcription factor. The Plant Journal 56, 73-85.
84. Sanders A, Collier R, Trethewy A, Gould G, Sieker R, Tegeder M. 2009. AAP1 regulates import of amino acids into developing Arabidopsis embryos. The Plant Journal 59, 540-552.
85. 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 Physiology 136, 2483-2499. (Pubitemid 41071292)
86. Schmidt R, Stransky H, Koch W. 2007. The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226, 805-813. (Pubitemid 47283072)
87. Schofield RA, Bi YM, Kant S, Rothstein SJ. 2009. Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant, Cell and Environment 32, 271-285.
88. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG. 2008. Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnology Journal 6, 722-732.
89. Slavikova S, Shy G, Yao YL, Giozman R, Levanony H, Pietrokovski S, Elazar Z, Galili G. 2005. The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. Journal of Experimental Botany 56, 2839-2849. (Pubitemid 41507221)
90. Smalle J, Vierstra RD. 2004. The ubiquitin 26S proteasome proteolytic pathway. Annual Review of Plant Biology 55, 555-590. (Pubitemid 38940944)
91. Stacey MG, Koh S, Becker J, Stacey G. 2002. AtOPT3, a member of the oligopeptide transporter family, is essential for embryo development in Arabidopsis. The Plant Cell 14, 2799-2811. (Pubitemid 35326305)
92. Tabuchi M, Abiko T, Yamaya T. 2007. Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). Journal of Experimental Botany 58, 2319-2327. (Pubitemid 47216540)
93. Tabuchi M, Sugiyama K, Ishiyama K, Inoue E, Sato T, Takahashi H, Yamaya T. 2005. Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. The Plant Journal 42, 641-651. (Pubitemid 40809883)
94. Tao Y, Marzluf GA. 1999. The NIT2 nitrogen regulatory protein of Neurospora: expression and stability of nit-2 mRNA and protein. Current Genetics 36, 153-158. (Pubitemid 29440498)
95. Tilsner J, Kassner N, Struck C, Lohaus G. 2005. Amino acid contents and transport in oilseed rape (Brassica napus L.) under different nitrogen conditions. Planta 221, 328-338. (Pubitemid 40876628)
96. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK. 2007. Nitrate transporters and peptide transporters. FEBS Letters 581, 2290-2300.
97. 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. The Plant Cell 12, 1491-1509.
98. Wang R, Okamoto M, Xing X, Crawford NM. 2003. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulphate metabolism. Plant Physiology 132, 556-567. (Pubitemid 36715057)
99. Wang RC, Xing XJ, Wang Y, Tran A, Crawford NM. 2009. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiology 151, 472-478.
100. Wingler A, Purdy S, MacLean JA, Pourtau N. 2006. The role of sugars in integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany 57, 391-399. (Pubitemid 43063791)
101. Yaeno T, Iba K. 2008. BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiology 148, 1032-1041. (Pubitemid 352847561)
102. Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proceedings of the National Academy of Sciences, USA 101, 7833-7838. (Pubitemid 38658114)
103. Zhang HM, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409. (Pubitemid 28063380)
104. Zhang HM, Forde BG. 2000. Regulation of Arabidopsis root development by nitrate availability. Journal of Experimental Botany 51, 51-59. (Pubitemid 30065411)
105. Zhang HM, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences, USA 96, 6529-6534. (Pubitemid 29256700)
106. Zhang Q. 2007. Strategies for developing Green Super Rice. Proceedings of the National Academy of Sciences, USA 104, 16402-16409. (Pubitemid 350211038)
107. Zhang YY, Xie Q. 2007. Ubiquitination in abscisic acid-related pathway. Journal of Integrative Plant Biology 49, 87-93. (Pubitemid 46055979)
108. Zimmermann P, Zentgraf U. 2005. The correlation between oxidative stress and leaf senescence during plant development. Cellular and Molecular Biology Letters 10, 515-534. (Pubitemid 41564522)