Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid

Science Signaling

Volumn 8, Issue 375, 2015, Pages

  Léran, Sophie ^a   Edel, Kai H ^b   Pervent, Marjorie ^a   Hashimoto, Kenji ^b,c   Corratge Faillie, Claire ^a   Offenborn, Jan Niklas ^b   Tillard, Pascal ^a   Gojon, Alain ^a   Kudla, Jörg ^b   Lacombe, Benoît ^a  

^a CNRS   (France)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; NITRATE; PHOSPHOTRANSFERASE; PROTEIN ABI2; PROTEIN CBL1; PROTEIN CIPK23; PROTEIN KINASE; UNCLASSIFIED DRUG; ABI2 PROTEIN, ARABIDOPSIS; ANION TRANSPORT PROTEIN; NITRIC ACID DERIVATIVE; NRT1.1 PROTEIN, ARABIDOPSIS; PHOSPHOPROTEIN PHOSPHATASE; VEGETABLE PROTEIN;

ANIMAL CELL; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GENE EXPRESSION; NITRATE UPTAKE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROOT DEVELOPMENT; XENOPUS; ACTIVE TRANSPORT; ANIMAL; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; XENOPUS LAEVIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; ANIMALS; ANION TRANSPORT PROTEINS; ARABIDOPSIS; BIOLOGICAL TRANSPORT, ACTIVE; NITRATES; PHOSPHOPROTEIN PHOSPHATASES; PLANT PROTEINS; STRESS, PHYSIOLOGICAL; XENOPUS LAEVIS;

EID: 84929084003     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaa4829     Document Type: Article

References (55)

1. H. Daniel, Molecular and integrative physiology of intestinal peptide transport. Annu. Rev. Physiol. 66, 361-384 (2004).
2. M. A. Hediger, M. F. Romero, J.-B. Peng, A. Rolfs, H. Takanaga, E. A. Bruford, The ABCs of solute carriers: Physiological, pathological and therapeutic implications of human membra ne transport proteins. Pflügers Arch. 447, 465-468 (2004).
3. H. Daniel, B. Spanier, G. Kottra, D. Weitz, From bacteria to man: Archaic protondependent peptide transporters at work. Physiology 21, 93-102 (2006).
4. Y. Boursiac, S. Lé ran, C. Corratgé-Faillie, A. Gojon, G. Krouk, B. Lacombe, ABA transport and transporters. Trends Plant Sci. 18, 325- 333 (2013).
5. S. Lé ran, K. Varala, J.-C. Boyer, M. Chiurazzi, N. Crawford, F. Daniel-Vedèle, L. David, R. Dickstein, E. Fernandez, B. Forde, W. Gassmann, D. Geiger, A. Gojon, J.-M. Gong , B. A. Halkier, J. M. Harris, R. Hedrich, A. M. Limami, D. Rentsch, M. Seo, Y.-F. Tsay, M. Zhang, G. Coruzzi, B. Lacombe, A unified nomenclature of nitrate transporter 1/peptide transporter family members in p lants. Trends Plant Sci. 19, 5- 9 (2014).
6. H. Saito T. Oikawa S. Hamamoto Y. Ishimaru M. Kanamori-Sato Y. Sasaki-Sekimoto T. Utsumi J. Chen Y. Kanno S. Masuda Y. Kamiya M. Seo N. Uozumi M. Ueda H. Ohta The jasmonate-responsive GTR1 transporter is required for gibberellinmediated stamen development in Arabidopsis. Nat. Commun. 6 6095(2015).
7. Y. Chiba, T. Shimizu, S. Miyakawa, Y. Kanno, T. Koshiba, Y. Kamiya, M. Seo, Identification of Arabidopsis thaliana NRT1/PTR family (NPF) proteins capable of transporting plant hormones. J. Plant Res. 10.1007/s10265-015- 0710-2 (2015).
8. N. M. Crawford, Nitrate: Nutrient and signal for plant growth. Plant Cell 7, 859-868 (1995).
9. G. Krouk, N. M. Crawford, G. M. Coruzzi, Y.-F. Tsay, Nitrate signaling: Adaptation to fluctuating environments. Curr. Opin. Plant Biol. 13, 265- 272 (2010).
10. E. A. Vidal, R. A. Gutiérrez, A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr. Opin. Plant Biol. 11, 521-529 (2008).
11. A. Krapp, L. C. David, C. Chardin, T. Girin, A. Marmagne, A.-S. Leprince, S. Chaillou, S. Ferrario-Mé ry, C.Meyer, F. Daniel-Vedele, Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 65, 789- 798 (2014).
12. S. Muños, C. C azettes, C. Fizames, F. Gaymard, P. Tillard, M. Lepetit, L. Lejay, A. Gojon, Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transp orter, NRT2.1. Plant Cell 16, 2433-2447 (2004).
13. T. Remans, P. Nacry, M. Pervent, S. Filleur, E. Diatloff, E. Mounier, P. Tillard, B. G. Forde, A. Gojon, The Arabidopsis NRT 1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl. Acad. Sci. U.S.A. 103, 19206-19211 (2006).
14. G. Krouk, B. Lacombe, A. Bielach, F. P errine-Walker, K. Malinska, E. Mounier, K. Hoyerova, P. Tillard, S. Leon, K. Ljung, E. Zazimalova, E. Benkova, P. Nacry, A. Gojon, Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient se nsing in plants. Dev. Cell 18, 927- 937 (2010).
15. C. H. Ho, S. H. Lin, H. C. Hu, Y. F. Tsay, CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194 (2009).
16. E. Mounier, M. Pervent, K. Ljung, A. Gojon, P. Nacry, Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant Cell Environ. 37, 162- 174 (2013).
17. S. Lé ran, S. Muños, C. Brachet, P. Tillard, A. Gojon, B. Lacombe, Arabidopsis NRT1.1 is a bidirectional transporter involved in root-to-shoot nitrate translocation. Mol. Plant 6, 1984-1987 (2013).
18. E. Bouguyon, F. Brun, D. Meynard, M. Kubes,M.Pervent,S. Leran, B. Lacombe, G. Krouk, E. Guiderdoni, E. Za?ímalová, K. Hoyerová , P. Nacry, A. Gojon, Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1, 1-8 (2015).
19. R. Wang, X. Xing, Y. Wang, A. Tran, N. M. Crawford, A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol. 151, 472-478 (2009).
20. G. Krouk, D. Tranchina, L. Lejay, A. A. Cruikshank, D. Shasha, G. M. Coruzzi, R. A. Gutiérrez, A systems approach uncovers restrictions for sign al interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLOS Comput. Biol. 5, e1000326 (2009).
21. N.-C. Huang, C.-S. Chiang, N. M. Crawford, Y.-F. Tsay, CHL1 encodes a co mponent of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8, 2183-2191 (1996).
22. K.-H. Liu, C.-Y. Huang, Y.-F. Tsay, CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11, 865-874 (1999).
23. K.-H. Liu, Y.-F. Tsay, Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22, 1005-1013 (2003).
24. C.-H. Ho, Y.-F. Tsay, Nitrate, ammonium, and potassium sensing and signaling. Curr. Opin. Plant Biol. 13, 604- 610 (2010).
25. Y.-Y. Wang, P.-K. Hsu, Y.-F. Tsay, Uptake, allocation and signaling of nitrate. Trends Plant Sci. 17, 458- 467 (2012).
26. A. D. Glass, Z. Kotur, A reevaluation of the role of Arabidopsis NRT1.1 in high-affinity nitrate transport. Plant Physiol. 163, 1103- 1106 (2013).
27. S. Weinl J. Kudla. The CBL-CIPK Ca2+-decoding signaling network: Function and perspectives. New Phytol.184. 517-528(2009).
28. V. Albrecht, O. Ritz, S. Linder, K. Har ter, J. Kudla, The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J. 20, 1051-1063 (2001).
29. O. Batisti?, J. Kudla, Analysis of calcium signaling pathways in plants. Biochim. Biophys. Acta 1820, 1283- 1293 (2012).
30. J. Xu, H.-D. Li, L.-Q. Chen, Y. Wang, L.-L. Liu, L. He, W.-H. Wu, A protein kinase, interacting with two cal cineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125, 1347-1360 (2006).
31. S. C. Lee,W.-Z. Lan, B.-G. Kim, L. Li, Y. H. Cheong, G. K. Pandey, G. Lu, B. B. Buch anan, S. Luan, A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc. Natl. Acad. Sci. U.S.A. 104, 15959-15964 (2007).
32. K. Held, F. Pascaud, C. Eckert, P. Gajdanowicz, K. Hashimoto, C. Corratgé-Faillie, J. N. Offenborn, B. Lacombe, I. Dreyer, J.-B. Thibaud, J. Kudla, Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 c alcium sensor/protein kinase complex. Cell Res. 21, 1116- 1130 (2011).
33. Y.-F. Tsay, J. I. Schroeder, K. A. Feldmann, N. M. Crawford, The herbicide sensitivity gene CHL1 of Arabidopsis en codes a nitrate-inducible nitrate transporter. Cell 72, 705-713 (1993).
34. A. Schweighofer, H. Hirt, I. Meskiene, Plant PP2C phosphatases: Emerging functions in stress signaling. Trends Plant Sci. 9, 236-243 (2004).
35. A. Medici, G. Krouk, The primary nitrate response: A multifaceted signalling pathway. J. Exp. Bot. 65, 5567- 5576 (2014).
36. K. Hashimoto, C. Eckert, U. Anschü tz, M. Scholz, K. Held, R. Waadt, A. Reyer, M. Hippler, D. Becker, J. Kudla, Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-int eracting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. J. Biol. Chem. 287, 7956- 7968 (2012).
37. P. Nacry, E. Bouguyon, A. Gojon, Nitrogen acquisition by roots: Physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370, 1-29 (2013).
38. Y. H. Cheong, G. K. Pandey, J. J. Grant, O. Batistic, L. Li, B.-G. Kim, S.-C. Lee, J. Kudla, S. Luan, Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 52, 223-239 (2007).
39. T. Maierhofer, M. Diekmann, J. N. Offenborn, C. Lind, H. Bauer, K. Hashimoto, K. A. S. Al-Rasheid, S. Luan, J. Kudla, D. Geiger, R. Hedrich, Site- and ki nase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci. Signal. 7, ra86 (2014).
40. I. De Smet, L. Signora, T. Beeckman, D. Inzé, C. H. Foye r, H. Zhang, An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33, 543-555 (2003).
41. L. Signora, I. De Smet, C. H. Foyer, H. Zhang, ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. 28, 655-662 (2002).
42. W.-Z. Lan, S.-C. Lee, Y.-F. Che, Y.-Q. Jiang, S. Luan, Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions. Mol. Plant 4, 527-536 (2011).
43. M. Ohta, Y. Guo, U. Halfter, J.-K. Zhu, A novel domain in the protein kinase SOS2 medi ates interaction with the protein phosphatase 2C ABI2. Proc. Natl. Acad. Sci. U.S.A. 100, 11771-11776 (2003).
44. W. J. Lyzenga, H. Liu, A. Schofield, A. Muise-Hennessey, S. L. Stone, Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J. Exp. Bot. 64, 2779- 2791 (2013).
45. A. Joshi-Saha, C. Valon, J. Leung, A brand new START: Abscisic acid perception and transduction in the guard cell. Sci. Signal. 4, re4 (2011).
46. E. R. Liman, J. Tytgat, P. Hess, Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9, 861-871 (1992).
47. D. Geiger, S. Scherzer, P. Mumm, A. Stange, I. Marten, H. Bauer, P. Ache, S. Matschi, A. Liese, K. A. Al-Rasheid, T. Romeis, R. Hedrich, Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phospha tase pair. Proc. Natl. Acad. Sci. U.S.A. 106, 21425-21430 (2009).
48. N. Leonhardt, J. M. Kwak, N. Robert, D. Waner, G. Leonhardt, J. I. Schroeder, Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16, 596-615 (2004).
49. J. M. Kuhn A. Boisson-Dernier M. B. Dizon M. H. Maktabi J. I. Schroeder. The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 140 127-139(2006).
50. S. Rubio, A. Rodrigues, A. Saez, M. B. Dizon, A. Galle, T.-H. Kim, J. Santiago, J. Flexas, J. I. Schroeder, P. L. Rodriguez, Triple loss of function of protein phosphatases type 2C leads to parti al constitutive response to endogenous abscisic acid. Plant Physiol. 150, 1345-1355 (2009).
51. M. Walter, C. Chaban, K. Schütze, O. Batistic, K. Weckermann, C. Näke, D. Blazevic, C. G refen, K. Schumacher, C. Oecking, K. Harter, J. Kudla, Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438 (2004).
52. O. Batisti?, R. Waadt, L. Steinhorst, K. Held, J. Kudla, CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 61, 211-222 (2010).
53. O. Batisti?, N. Sorek, S. Schn ültke, S. Yalovsky, J. Kudla, Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20, 1346-1362 (2008 ).
54. R. Waadt, L. K. Schmidt, M. Lohse, K. Hashimoto, R. Bock, J. Kudla, Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. P lant J. 56, 505-516 (2008).
55. G. Krouk, P. Mirowski, Y. LeCun, D. E. Shasha, G. M. Coruzzi, Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol. 11, R123 (2010).