The Primary Nitrate Response: A multifaceted signalling pathway

Journal of Experimental Botany

Volumn 65, Issue 19, 2014, Pages 5567-5576

  Medici, Anna ^a   Krouk, Gabriel ^a  

^a CNRS   (France)

Author keywords

CHL1 NRT1.1 mutations; LBD37 38; Nitrate (NO3 ); NLP7; Nutritional environment; Primary Nitrate Response (PNR)

Indexed keywords

ANION TRANSPORT PROTEIN; ARABIDOPSIS PROTEIN; NITRIC ACID DERIVATIVE; NITROGEN;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; META ANALYSIS; METABOLISM; MUTATION; PHYSIOLOGY; PLANT ROOT; SIGNAL TRANSDUCTION;

ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MUTATION; NITRATES; NITROGEN; PLANT ROOTS; SIGNAL TRANSDUCTION;

EID: 84929075968     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru245     Document Type: Review

References (50)

1. Alboresi A, Gestin C, Leydecker MT, Bedu M, Meyer C, Truong HN. 2005. Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant, Cell and Environment 28, 500-512.
2. Alvarez JM, Vidal EA, Gutierrez RA. 2012. Integration of local and systemic signaling pathways for plant N responses. Current Opinion in Plant Biology 15, 185-191.
3. Burger G, Tilburn J, Scazzocchio C. 1991. Molecular cloning and functional characterization of the pathway-specific regulatory gene nirA, which controls nitrate assimilation in Aspergillus nidulans. Molecular and Cellular Biology 11, 795-802.
4. Camargo A, Llamas A, Schnell RA, Higuera JJ, Gonzalez-Ballester D, Lefebvre PA, Fernandez E, Galvan A. 2007. Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. The Plant Cell 19, 3491-3503.
5. 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.
6. Castro Marín I, Loef I, Bartetzko L, Searle I, Coupland G, Stitt M, Osuna D. 2011. Nitrate regulates foral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways. Planta 233, 539-552.
7. Cavicchioli R, Chiang RC, Kalman LV, Gunsalus RP. 1996. Role of the periplasmic domain of the Escherichia coli NarX sensor-transmitter protein in nitrate-dependent signal transduction and gene regulation. Molecular Microbiology 21, 901-911.
8. Chai W, Stewart V. 1998. NasR, a novel RNA-binding protein, mediates nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader in vitro. Journal of Molecular Biology 283, 339-351.
9. Chiang RC, Cavicchioli R, Gunsalus RP. 1997. 'Locked-on' and 'locked-off' signal transduction mutations in the periplasmic domain of the Escherichia coli NarQ and NarX sensors affect nitrate- and nitritedependent regulation by NarL and NarP. Molecular Microbiology 24, 1049-1060.
10. Crawford NM, Glass ADM. 1998. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389-395.
11. Forde BG, Walch-Liu P. 2009. Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell and Environment 32, 682-693.
12. Fu YH, Kneesi JY, Marzluf GA. 1989. Isolation of nit-4, the minor nitrogen regulatory gene which mediates nitrate induction in Neurospora crassa. Journal of Bacteriology 171, 4067-4070.
13. + transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. The Plant Journal 26, 143-155.
14. 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 Molecular Biology 18, 55-64.
15. Gutierrez RA, Gifford ML, Poultney C, Wang R, Shasha DE, Coruzzi GM, Crawford NM. 2007. Insights into the genomic nitrate response using genetics and the Sungear Software System. Journal of Experimental Botany 58, 2359-2367.
16. Ho CH, Lin SH, Hu HC, Tsay YF. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
17. 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.
18. Konishi M, Yanagisawa S. 2013. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nature Communications 4, 1617.
19. Krouk G, Crawford NM, Coruzzi GM, Tsay YF. 2010a. Nitrate signaling: adaptation to fuctuating environments. Current Opinion in Plant Biology 13, 266-273.
20. Krouk G, Lacombe B, Bielach A et al. 2010b. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18, 927-937.
21. Krouk G, Lingeman J, Colon AM, Coruzzi G, Shasha D. 2013. Gene regulatory networks in plants: learning causality from time and perturbation. Genome Biology 14, 123.
22. Krouk G, Mirowski P, Le Cun Y, Shasha DE, Coruzzi GM. 2010c. Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biology 11, R123.
23. 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 in Plant Science 16, 178-182.
24. - demand signaling in Arabidopsis. Plant Physiology 142, 1075-1086.
25. 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, e1000326.
26. - uptake systems by N- and C-status of Arabidopsis plants. The Plant Journal 18, 509-519.
27. Leran S, Varala K, Boyer JC et al. 2014. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends in Plant Science 19, 5-9.
28. Liu KH, Tsay YF. 2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. The EMBO Journal. 22, 1005-1013.
29. Marchive C, Roudier F, Castaings L, Brehaut V, Blondet E, Colot V, Meyer C, Krapp A. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications 4, 1713.
30. Muños S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A. 2004. Transcript profling 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. The Plant Cell 16, 2433-2447.
31. Nacry P, Bouguyon E, Gojon A. 2013. Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant and Soil 370, 1-29.
32. Obertello M, Krouk G, Katari MS, Runko SJ, Coruzzi GM. 2010. Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis. BMC Systems Biology 4, 111.
33. Poultney CS, Gutierrez RA, Katari MS, Gifford ML, Paley WB, Coruzzi GM, Shasha DE. 2007. Sungear: interactive visualization and functional analysis of genomic datasets. Bioinformatics 23, 259-261.
34. --induced stimulation of leaf growth. Journal of Experimental Botany 56, 1143-1152.
35. 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 nitraterich patches. Proceedings of the National Academy of Sciences, USA 103, 19206-19211.
36. 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. The Plant Cell 21, 3567-3584.
37. Ruffel S, Freixes S, Balzergue S et al. 2008. Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiology 146, 2020-2035.
38. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM. 2011. Nitrogen economics of root foraging: transitive closure of the nitratecytokinin relay and distinct systemic signaling for N supply vs. demand. Proceedings of the National Academy of Sciences, USA 108, 18524-18529.
39. 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. The Plant Cell 9, 783-798.
40. Schnell RA, Lefebvre PA. 1993. Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134, 737-747.
41. Tian QY, Sun P, Zhang WH. 2009. Ethylene is involved in nitratedependent root growth and branching in Arabidopsis thaliana. New Phytologist 184, 918-931.
42. 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.
43. Vidal EA, Gutierrez RA. 2008. A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Current Opinion in Plant Biology 11, 521-529.
44. Walch-Liu P, Forde BG. 2008. Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. The Plant Journal 54, 820-828.
45. Wang JW, Czech B, Weigel D. 2009a. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749.
46. 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 Physiology 136, 2512-2522.
47. Wang R, Xing X, Crawford N. 2007. Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiology 145, 1735-1745.
48. Wang R, Xing X, Wang Y, Tran A, Crawford NM. 2009b. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiology 151, 472-478.
49. Wilkinson J, Crawford N. 1993. Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Molecular and General Genetics 239, 289-297.
50. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409.