The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis

Plant Physiology

Volumn 169, Issue 2, 2015, Pages 1397-1404

  Riveras, Eleodoro ^a   Alvarez, José M ^a   Vidal, Elena A ^a   Oses, Carolina ^a   Vega, Andrea ^a   Gutiérrez, Rodrigo A ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ANION TRANSPORT PROTEIN; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE; NITRIC ACID DERIVATIVE; NRT1.1 PROTEIN, ARABIDOPSIS; PHOSPHATIDYLINOSITOL; PHOSPHOLIPASE C; PLANT PROTEIN;

ARABIDOPSIS; CALCIUM SIGNALING; CYTOSOL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT ROOT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ANION TRANSPORT PROTEINS; ARABIDOPSIS; CALCIUM; CALCIUM SIGNALING; CYTOSOL; GENE EXPRESSION REGULATION, PLANT; INOSITOL 1,4,5-TRISPHOSPHATE; NITRATES; PHOSPHATIDYLINOSITOLS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

EID: 84942889518     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00961     Document Type: Article

References (59)

1. Aceituno FF, Moseyko N, Rhee SY, Gutiérrez RA (2008) The rules of gene expression in plants: organ identity and gene body methylation are key factors for regulation of gene expression in Arabidopsis thaliana. BMC Genomics 9: 438
2. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20: 1051-1063
3. Alexandra J, Lassalles JP, Kado RT (1999) Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1,4,5-trisphosphate. Nature 343: 567-570
4. Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras-López O, Tamayo KP, Aceituno F, Gómez I, Ruffel S, Lejay L, et al (2014) Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J 80: 1-13
5. Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M, Leran S, Lacombe B, Krouk G, Guiderdoni E, Zazímalová E, et al (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat Plants 1: 1-8
6. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46: 95-122
7. Canales J, Moyano TC, Villarroel E, Gutiérrez RA (2014) Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front Plant Sci 5: 22
8. Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signalling network. J Exp Bot 62: 1391-1397
9. Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin- induced lateral root formation in rice. Protoplasma 249: 187-195
10. Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to- shoot signaling in plants. Proc Natl Acad Sci USA 111: 6497-6502
11. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61: 593-620
12. 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
13. Furuichi T, Mori IC, Takahashi K, Muto S (2001) Sugar-induced increase in cytosolic Ca(2+) in Arabidopsis thaliana whole plants. Plant Cell Physiol 42: 1149-1155
14. Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Selfreporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134: 898-908
15. 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
16. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the fore-front of rapid systemic signaling. Trends Plant Sci 19: 623-630
17. Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor (s) in plants. J Exp Bot 62: 2299-2308
18. Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, et al (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci USA 105: 4939-4944
19. Harper JF, Breton G, Harmon A (2004) Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol 55: 263-288
20. Heilmann I, Perera IY (2013) Measurement of inositol (1,4,5) trisphosphate in plant tissues by a competitive receptor binding assay. Methods Mol Biol 1009: 33-41
21. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17: 2142-2155
22. Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55: 401-427
23. Hirose K, Kadowaki S, Tanabe M, Takeshima H, Iino M (1999) Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns. Science 284: 1527-1530
24. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194
25. Ho CH, Tsay YF (2010) Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13: 604-610
26. Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, Welti R, Wang X (2009) Phospholipase D epsilon and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J 58: 376-387
27. 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
28. Hunt L, Otterhag L, Lee JC, Lasheen T, Hunt J, Seki M, Shinozaki K, Sommarin M, Gilmour DJ, Pical C, et al (2004) Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. New Phytol 162: 643-654
29. Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. Plant J 26: 595-605
30. Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8: 489-503
31. Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5: 332-338
32. Lemtiri-Chlieh F, MacRobbie EAC, Webb AAR, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 100: 10091-10095
33. Meijer HJG, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54: 265-306
34. Michal Johnson J, Reichelt M, Vadassery J, Gershenzon J, Oelmüller R (2014) An Arabidopsis mutant impaired in intracellular calcium elevation is sensitive to biotic and abiotic stress. BMC Plant Biol 14: 162
35. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6: 227-233
36. Munnik T, Vermeer JEM (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33: 655-669
37. Nagata T, Iizumi S, Satoh K, Ooka H, Kawai J, Carninci P, Hayashizaki Y, Otomo Y, Murakami K, Matsubara K, et al (2004) Comparative analysis of plant and animal calcium signal transduction element using plant full-length cDNA data. Mol Biol Evol 21: 1855-1870
38. Polisensky DH, Braam J (1996) Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol 111: 1271-1279
39. Reddy VS, Reddy ASN (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65: 1745-1776
40. 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: 837-843
41. Sanchez JP, Chua NH (2001) Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 13: 1143-1154
42. Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11: 691-706
43. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell (Suppl) 14: S401-S417
44. Sang Y, Cui D, Wang X (2001) Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiol 126: 1449-1458
45. Stoelzle S, Kagawa T, Wada M, Hedrich R, Dietrich P (2003) Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc Natl Acad Sci USA 100: 1456-1461
46. 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: 1015-1019
47. Tasma IM, Brendel V, Whitham SA, Bhattacharyya MK (2008) Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem 46: 627-637
48. Trewavas AJ, Malhó R (1998) Ca2+ signalling in plant cells: the big net-work! Curr Opin Plant Biol 1: 428-433
49. Vidal EA, Álvarez JM, Gutiérrez RA (2014) Nitrate regulation of AFB3 and NAC4 gene expression in Arabidopsis roots depends on NRT1.1 nitrate transport function. Plant Signal Behav 9: e28501
50. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107: 4477–4482
51. Vidal EA, Gutiérrez RA (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11: 521–529
52. Vidal EA, Moyano TC, Krouk G, Katari MS, Tanurdzic M, McCombie WR, Coruzzi GM, Gutiérrez RA (2013a) Integrated RNA-seq and sRNA-seq analysis identifies novel nitrate-responsive genes in Arabidopsis thaliana roots. BMC Genomics 14: 701
53. Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA (2013b) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110: 12840–12845
54. 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
55. Wang R, Tischner R, Gutiérrez 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
56. 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
57. Wang X, Bian Y, Cheng K, Zou H, Sun SSM, He JX (2012) A comprehensive differential proteomic study of nitrate deprivation in Arabidopsis reveals complex regulatory networks of plant nitrogen responses. J Proteome Res 11: 2301–2315
58. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92: 487–511
59. Zheng SZ, Liu YL, Li B, Shang ZL, Zhou RG, Sun DY (2012) Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J 69: 689–700