Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 16196-16201

  Xia, Jinchan ^a   Kong, Dongdong ^b   Xue, Shaowu ^c   Tian, Wang ^a   Li, Nan ^a   Bao, Fang ^a   Hu, Yong ^a   Du, Jing ^a   Wang, Yu ^a   Pan, Xiaojun ^a   Wang, Lei ^a   Zhang, Xiaochen ^a   Niu, Guoqi ^a   Feng, Xue ^a   Li, Legong ^a   He, Yikun ^a  

^a CAPITAL NORMAL UNIVERSITY   (China)

^b Bldg 142   (United States)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Electrophysiological studies; Genetic approach; Potassium nutrition

Indexed keywords

AKT1 PROTEIN; NITRIC OXIDE; POTASSIUM; PROTEIN KINASE B; PYRIDOXAL 5 PHOSPHATE; PYRIDOXINE; SODIUM; UNCLASSIFIED DRUG; AKT1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; POTASSIUM CHANNEL;

ABSORPTION; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; ENZYME ACTIVITY; GENE EXPRESSION; HOMEOSTASIS; LOWER PLANT; NONHUMAN; PLANT GROWTH; PLANT ROOT; POTASSIUM TRANSPORT; PROTOPLAST; XENOPUS; ANIMAL; CYTOLOGY; GENETICS; ION TRANSPORT; METABOLISM; OOCYTE; PHYSIOLOGY; XENOPUS LAEVIS;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; HOMEOSTASIS; ION TRANSPORT; NITRIC OXIDE; OOCYTES; PLANT ROOTS; POTASSIUM; POTASSIUM CHANNELS; PROTOPLASTS; PYRIDOXAL PHOSPHATE; VITAMIN B 6; XENOPUS LAEVIS;

EID: 84909606336     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417473111     Document Type: Article

References (64)

1. ͆írová J, Sedlářová M, Piterková J, Luhová L, Petřivalský M (2011) The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci 181(5):560-572.
2. Bethke PC, Libourel IG, Reinöhl V, Jones RL (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223(4):805-812.
3. Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129(3):954-956.
4. Mishina TE, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ 30(1):39-52.
5. Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17(12):3436-3450.
6. He Y, et al. (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305(5692):1968-1971.
7. Neill S, et al. (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59(2):165-176.
8. García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126(3):1196-1204.
9. Ramirez L, Simontacchi M, Murgia I, Zabaleta E, Lamattina L (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: A well equipped team to preserve plant iron homeostasis. Plant Sci 181(5):582-592.
10. Graziano M, Lamattina L (2005) Nitric oxide and iron in plants: An emerging and converging story. Trends Plant Sci 10(1):4-8.
11. Terrile MC, et al. (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70(3):492-500.
12. Ribeiro DM, et al. (2009) Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ 32(1):46-57.
13. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12(4):451-458.
14. Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: The versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109-136.
15. Bai X, et al. (2011) Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J Proteome Res 10(10):4349-4364.
16. Wang H, Liang X, Wan Q, Wang X, Bi Y (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230(2):293-307.
17. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6(5):441-445.
18. Chen J, et al. (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30(12):1570-1585.
19. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144(1):206-217.
20. Zhang Y, et al. (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224(3):545-555.
21. Molassiotis A, Tanou G, Diamantidis G (2010) NO says more than 'YES' to salt tolerance: Salt priming and systemic nitric oxide signaling in plants. Plant Signal Behav 5(3):209-212.
22. Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: Evidence for a critical role of potassium nutrition. Plant Cell 10(7):1181-1191.
23. Hirsch RE, Lewis BD, Spalding EP, Sussman MR (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280(5365):918-921.
24. Sentenac H, et al. (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256(5057):663-665.
25. Rubio F, Santa-Maria GE, Rodriguez-Navarro A (2000) Cloning of Arabidopsis and barley cDNAs encoding HAK potassium transporters in root and shoot cells. Physiol Plant 109(1):34-43.
26. Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2011) Root K+ acquisition in plants: The Arabidopsis thaliana model. Plant Cell Physiol 52(9):1603-1612.
27. Pyo YJ, Gierth M, Schroeder JI, Cho MH (2010) High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol 153(2):863-875.
28. Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451-476.
29. + nutrition. Plant J 9(2):195-203.
30. Xu J, et al. (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125(7):1347-1360.
31. + channel from Arabidopsis thaliana. J Biol Chem 271(37):22863-22870.
32. + channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103(33):12625-12630.
33. Lee SC, et al. (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci USA 104(40):15959-15964.
34. + stress. Cell Res 20(7):826-837.
35. Geiger D, et al. (2009) Heteromeric AtKC1·AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions. J Biol Chem 284(32):21288-21295.
36. Shi H, Xiong L, Stevenson B, Lu T, Zhu JK (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 14(3):575-588.
37. González E, Danehower D, Daub ME (2007) Vitamer levels, stress response, enzyme activity, and gene regulation of Arabidopsis lines mutant in the pyridoxine/pyridoxamine 5'-phosphate oxidase (PDX3) and the pyridoxal kinase (SOS4) genes involved in the vitamin B6 salvage pathway. Plant Physiol 145(3):985-996.
38. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50(3):413-492.
39. Libourel IG, Bethke PC, De Michele R, Jones RL (2006) Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: Use of a flow-through apparatus for delivery of nitric oxide. Planta 223(4):813-820.
40. Fitzpatrick TB, et al. (2012) Vitamin deficiencies in humans: Can plant science help? Plant Cell 24(2):395-414.
41. Tambasco-Studart M, et al. (2005) Vitamin B6 biosynthesis in higher plants. Proc Natl Acad Sci USA 102(38):13687-13692.
42. Chen H, Xiong L (2005) Pyridoxine is required for post-embryonic root development and tolerance to osmotic and oxidative stresses. Plant J 44(3):396-408.
43. Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50(10):1238-1246.
44. Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8(4):390-396.
45. Cheong YH, et al. (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52(2):223-239.
46. Chérel I (2004) Regulation of K+ channel activities in plants: From physiological to molecular aspects. J Exp Bot 55(396):337-351.
47. Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258(5088):1654-1658.
48. Mur LA, et al. (2013) Nitric oxide in plants: An assessment of the current state of knowledge. AoB Plants 5: pls052.
49. Sokolovski S, Blatt MR (2004) Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol 136(4):4275-4284.
50. 2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J 43(4):520-529.
51. Garcia-Mata C, et al. (2003) Nitric oxide regulates K+ and Cl-channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100(19):11116-11121.
52. + transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3(2):326-333.
53. Rubio F, Alemán F, Nieves-Cordones M, Martínez V (2010) Studies on Arabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K uptake. Physiol Plant 139(2):220-228.
54. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168(4):521-530.
55. + antiporter under high salinity. PLoS ONE 8(8):e71543.
56. Zhao L, et al. (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134(2):849-857.
57. 2+ and protein kinases. J Exp Bot 59(2):155-163.
58. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóždž EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181(5):612-620.
59. He H, He L, Gu M (2012) Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Signal Behav 7(4):469-471.
60. Ballatori N, Truong AT, Jackson PS, Strange K, Boyer JL (1995) ATP depletion and inactivation of an ATP-sensitive taurine channel by classic ion channel blockers. Mol Pharmacol 48(3):472-476.
61. Hinz HR, Kirley TL (1990) Lysine 480 is an essential residue in the putative ATP site of lamb kidney (Na, K)-ATPase. Identification of the pyridoxal 5'-diphospho-5'-adenosine and pyridoxal phosphate reactive residue. J Biol Chem 265(18):10260-10265.
62. Palmgren MG (2001) Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817-845.
63. Fitzpatrick TB, et al. (2007) Two independent routes of de novo vitamin B6 biosynthesis: Not that different after all. Biochem J 407(1):1-13.
64. Tanaka T, Tateno Y, Gojobori T (2005) Evolution of vitamin B6 (pyridoxine) metabolism by gain and loss of genes. Mol Biol Evol 22(2):243-250.