Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in arabidopsis

Annals of Botany

Volumn 116, Issue 4, 2015, Pages 695-702

  Correa Aragunde, Natalia ^a   Cejudo, Francisco J ^b   Lamattina, Lorenzo ^a  

^a UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Arabidopsis thaliana; auxin; denitrosylation; nitric oxide; NTR; reactive nitrogen species; root growth; thioredoxin reductase

Indexed keywords

DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH RESPONSE; HORMONE; INHIBITION; NITRIC OXIDE; NITROGEN; PROTEIN; REDOX CONDITIONS; ROOT SYSTEM; SCAVENGING (CHEMISTRY); SEED TREATMENT; SEEDLING ESTABLISHMENT;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; NITRIC OXIDE; PHYTOHORMONE; THIOREDOXIN REDUCTASE;

ARABIDOPSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT ROOT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; INDOLEACETIC ACIDS; NITRIC OXIDE; PLANT GROWTH REGULATORS; PLANT ROOTS; THIOREDOXIN-DISULFIDE REDUCTASE;

EID: 84942279831     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcv116     Document Type: Article

References (55)

1. Alkhalfioui F, Renard M, Frendo P, et al. (2008). A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiology 148: 424-435
2. Barroso JB, Corpas FJ, Carreras A, et al. (2006). Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. Journal of Experimental Botany 57: 1785-1793
3. Bashandy T, Guilleminot J, Vernoux T, et al. (2010). Interplay between the NADP-linked thioredoxin and glutathione systems in arabidopsis auxin signaling. The Plant Cell 22: 376-391
4. Benhar M, Forrester MT, Hess DT, Stamler JS. (2008). Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320: 1050-1054
5. Benhar M, Thompson JW, Moseley MA, Stamler JS. (2010). Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49: 6963-6969
6. Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G. (2002). Shoot-derived auxin is essential for early lateral root emergence in arabidopsis seedlings. The Plant Journal 29: 325-332
7. Chvanov M, Gerasimenko OV, Petersen OH, Tepikin AV. (2006). Calcium-dependent release of NO from intracellular S-nitrosothiols. EMBO Journal 25: 3024-3032
8. Correa-Aragunde N, Graziano M, Lamattina L (2004). Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218: 900-905
9. Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013). Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in arabidopsis. Journal of Experimental Botany 64: 3339-3349
10. Díaz M, Achkor H, Titarenko E, Martínez MC. (2003). The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Letters 543: 136-139
11. Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ. (2005). A central role for S-nitrosothiols in plant disease resistance. Proceedings of the National Academy of Science USA 102: 8054-8059
12. Flores T, Todd CD, Tovar-Mendez A, et al. (2008). Arginase-negative mutants of arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiology 147: 1936-1946
13. Frungillo L, Skelly MJ, Loake GJ, Spoel SH, Salgado I. (2014). S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nature Communications 5: 5401
14. Gelhaye E, Navrot N, Macdonald IK, Rouhier N, Raven EL, Jacquot JP. (2006). Ascorbate peroxidase-thioredoxin interaction. Photosynthesis Research 89: 193-200
15. Gromer S, Arscott LD, Williams CH, Schirmer RH, Becker K. (1998). Human placenta thioredoxin reductase isolation of the selenoenzyme, steady state kinetics, and inhibition by therapeutic gold compounds. Journal of Biological Chemistry 273: 20096-20101
16. Hewinson J, Moore SF, Glover C, Watts AG, MacKenzie AB. (2008). A key role for redox signaling in rapid P2X7 receptor-induced IL-1 beta processing in human monocytes. Journal of Immunology 180: 8410-8420
17. Holmgren A. (2008). Biochemistry. SNO removal. Science 320: 1019-1020
18. Ishikawa A, Kubota Y, Murayama T, Nomura Y. (1999). Cell death by 1-chloro-2, 4-dinitrobenzene, an inhibitor of thioredoxin reductase and its dual regulation by nitric oxide in rats. Neuroscience Letters 277: 99-102
19. Jaffrey SR, Snyder SH. (2001). The biotin switch method for the detection of S-nitrosylated proteins. Science STKE 86: pl1
20. Jefferson RA, Kavanagh TA, Bevan MW. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal. 6: 3901-3907
21. Jensen D, Belka G, Du Bois G. (1998). S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochemical Journal 331: 659-668
22. Jia J, Arif A, Terenzi F, Willard B, Plow E, Hazen S, Fox P. (2014). Target-selective protein S-nitrosylation by sequence motif recognition. Cell 159: 623-634
23. Kim SF, Huri DA, Snyder SH. (2005). Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 310: 1966-1970
24. Kirchsteiger K, Ferrández J, Pascual MB, González M, Cejudo FJ. (2012). NADPH thioredoxin reductase C is localized in plastids of photosynthetic and nonphotosynthetic tissues and is involved in lateral root formation in arabidopsis. The Plant Cell 24: 1534-1548
25. Kneeshaw S, Gelineau SR, Tada Y, Loake GJ, Spoel SH. (2014). Selective protein denitrosylation activity of thioredoxin h 5 modulates plant immunity. Molecular Cell 56: 153-162
26. Kolbert Z, Bartha B, Erdei L (2007). Exogenous auxin-induced NO synthesis is nitrate reductase-associated in arabidopsis thaliana root primordia. Journal of Plant Physiology 165: 967-975
27. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G. (2003). Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology 54: 109-136
28. Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E. (2008). Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in arabidopsis. The Plant Cell 20: 786-802
29. Lindermayr C, Durner J. (2009). S-Nitrosylation in plants: pattern and function. Journal of Proteomics 73: 1-9
30. Marchant A, Bhalerao R, Casimiro I, et al. (2002). AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. The Plant Cell 14: 589-597
31. Marchand C, Le MP, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P. (2004). New targets of arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4: 2696-2706
32. Marino SM, Gladyshev VN. (2010). Structural analysis of cysteine Snitrosylation: a modified acid-based motif and the emerging role of transnitrosylation. Journal ofMolecular Biology 395: 844-859
33. Mendez-Bravo A, Raya-Gonzalez J, Herrera-Estrella L, Lopez-Bucio J. (2010). Nitric oxide is involved in alkamide-induced lateral root development in arabidopsis. Plant Cell Physiology 51: 1612-1626
34. Meyer Y, Siala W, Bashandy T, Riondet C, Vignols F, Reichheld JP. (2008). Glutaredoxins and thioredoxins in plants. Biochimica et Biophysica Acta 1783: 589-600
35. Nikitovic D, Holmgren A. (1996). S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. Journal of Biological Chemistry 271: 19180-19185
36. Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002). Nitric oxide is required for root organogenesis. Plant Physiology 129: 954-956
37. Park JK, Kostka P. (1997). Fluorometric detection of biological S-nitrosothiols. Analytical Biochemistry 249: 61-66
38. Pulido P, Cazalis R, Cejudo FJ. (2009). An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. The Plant Journal 57: 132-145
39. Reichheld JP, Meyer E, Khafif M, Bonnard G, Meyer Y. (2005). AtNTRB is the major mitochondrial thioredoxin reductase in arabidopsis thaliana. FEBS Letters 579: 337-342
40. Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y. (2007). Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in arabidopsis development. The Plant Cell 19: 1851-1865
41. Rigobello MP, Scutari G, Folda A, Bindoli A. (2004). Mitochondrial thioredoxin reductase inhibition by gold(I) compounds and concurrent stimulation of permeability transition and release of cytochrome c. Biochemical Pharmacology 67: 689-696
42. Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC. (2007). S-nitrosoglutathione reductase affords protection against pathogens in arabidopsis, both locally and systemically. Plant Physiology 143: 1282-1292
43. Sakamoto A, Ueda M, Morikawa H. (2002). Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Letters 515: 20-24
44. Sengupta R, Ryter SW, Zuckerbraun BS, Tzeng E, Billiar TR, Stoyanovsky DA. (2007). Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 46: 8472-8483
45. Serrato AJS, Pérez-Ruiz JM, Spínola MC, Cejudo FJ. (2004). A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in arabidopsis thaliana. Journal of Biological Chemistry 279: 43821-43827
46. Shahpiri A, Svensson B, Finnie C. (2008). The NADPH-dependent thioredoxin reductase/thioredoxin system in germinating barley seeds: gene expression, protein profiles, and interactions between isoforms of thioredoxin h and thioredoxin reductase. Plant Physiology 146: 789-799
47. Smiri M, Nahida Jelalib N, Ghoul JE. (2013). Cadmium affects the NADP-thioredoxin reductase/thioredoxin system in germinating pea seeds. Journal of Plant Interactions 8: 125-133
48. Tada Y, Spoel SH, Pajerowska-Mukhtar K, et al. (2008). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321: 952-956
49. Tello D, Tarín C, Ahicart P, Bretón-Romero R, Lamas S, Martínez-Ruiz A. (2009). A fluorescence switch technique increases the sensitivity of proteomic detection and identification of S-nitrosylated proteins. Proteomics 9: 5359-5370
50. Terrile MC, Paris R, Calderon-Villalobos LI, et al. (2012). Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. The Plant Journal 70: 492-500
51. Vieira Dos SC, Rey P. (2006). Plant thioredoxins are key actors in the oxidative stress response. Trends in Plant Science 11: 329-334
52. Wang P, Du Y, Li Y, Ren D, Song CP. (2010). Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in arabidopsis. The Plant Cell 22: 2981-2998
53. Wilson AK, Pickett FB, Turner JC, Estelle M. (1990). A dominant mutation in arabidopsis confers resistance to auxin, ethylene and abscisic acid. Molecular and General Genetics 22: 377-383
54. Wu C, Parrott AM, Liu T, et al. (2011). Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. Journal of Proteomics 74: 2498-2509
55. Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T. (2004). Target proteins of the cytosolic thioredoxins in arabidopsis thaliana. Plant Cell and Physiology 45: 18-27