S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway

Nature Communications

Volumn 5, Issue , 2014, Pages

  Frungillo, Lucas ^a   Skelly, Michael J ^b   Loake, Gary J ^b   Spoel, Steven H ^b   Salgado, Ione ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; OXIDOREDUCTASE; S NITROSOGLUTATHIONE; S NITROSOGLUTATHIONE REDUCTASE 1; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; GLUTATHIONE REDUCTASE; NITRIC ACID DERIVATIVE; NITROGEN; S NITROSOTHIOL; S-NITROSOGLUTATHIONE REDUCTASE, ARABIDOPSIS;

CHEMICAL BONDING; ENZYME ACTIVITY; GROWTH RESPONSE; NITRIC OXIDE; NUTRIENT UPTAKE; PLANT COMMUNITY; REDOX CONDITIONS; SIGNALING;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GENE EXPRESSION; NITRATE UPTAKE; NITROGEN FIXATION; NITROGEN METABOLISM; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; ARABIDOPSIS; BIOLOGICAL MODEL; HOMEOSTASIS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GLUTATHIONE REDUCTASE; HOMEOSTASIS; MODELS, BIOLOGICAL; NITRATES; NITRIC OXIDE; NITROGEN; OXIDATION-REDUCTION; S-NITROSOTHIOLS; SIGNAL TRANSDUCTION;

EID: 84925240109     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6401     Document Type: Article

References (69)

1. Crawford, N. M. Nitrate: nutrient and signal for plant growth. Plant Cell 7, 859-868 (1995).
2. Tsay, Y. F., Chiu, C. C., Tsai, C. B., Ho, C. H. & Hsu, P. K. Nitrate transporters and peptide transporters. FEBS Lett. 581, 2290-22300 (2007).
3. Wang, Y. Y., Hsu, P. K. & Tsay, Y. F. Uptake, allocation and signalling of nitrate. Trends Plant Sci. 17, 458-467 (2012).
4. Dechorgnat, J. et al. From the soil to the seeds: the long journey of nitrate in plants. J. Exp. Bot. 62, 1349-1359 (2011).
5. Li, W. et al. Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol. 143, 425-433 (2007).
6. Liu, K. H., Huang, C. Y. & Tsay, Y. F. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11, 865-874 (1999).
7. Ho, C. H., Lin, S. H., Hu, H. C. & Tsay, Y. F. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194 (2009).
8. Sun, J. et al. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507, 73-77 (2014).
9. Parker, J. L. & Newstead, S. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507, 68-72 (2014).
10. Zheng, H., Wisedchaisri, G. & Gonen, T. Crystal structure of a nitrate/nitrite exchanger. Nature 497, 647-651 (2013).
11. Lea, P. J. in Plant Biochemistry and Molecular Biology (eds Lea, P. &Leegood, R. C.) 155-180 (John Wiley and Sons, 1993).
12. Martínez-Espinosa, R. M., Cole, J. A., Richardson, D. J. & Watmough, N. J. Enzymology and ecology of the nitrogen cycle. Biochem. Soc. Trans. 39, 175-178 (2011).
13. Einsle, O. & Kroneck, P. Structural basis of denitrification. Biol. Chem. 385, 875-883 (2004).
14. Wilkinson, J. & Crawford, N. Identification and characterization of a chlorateresistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol. Gen. Genet. 239, 289-297 (1993).
15. Lejay, L., Tillard, P., Lepetit, M. & Olive, F. Molecular and functional regulation of two NO3-uptake systems by N-and C-status of Arabidopsis plants. Plant J. 18, 509-519 (1999).
16. Muños, S. et al. Transcript profiling 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. Plant Cell 16, 2433-2447 (2004).
17. Salgado, I., Martínez, M. C., Oliveira, H. C. & Frungillo, L. Nitric oxide signaling and homeostasis in plants: a focus on nitrate reductase and S-nitrosoglutathione reductase in stress-related responses. Brazilian J. Bot. 32, 89-98 (2013).
18. Neill, S. et al. Nitric oxide evolution and perception. J. Exp. Bot. 59, 25-35 (2008).
19. Yamasaki, H., Sakihama, Y. & Takahashi, S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4, 128-129 (1999).
20. Rockel, P., Strube, F. & Rockel, A. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53, 103-110 (2002).
21. Modolo, L. V., Augusto, O., Almeida, I. M. G., Magalhaes, J. R. & Salgado, I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 579, 3814-3820 (2005).
22. Modolo, L. V. et al. Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci. 171, 34-40 (2006).
23. Mur, L. A. J. et al. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5, pls052 (2013).
24. He, Y. et al. Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968-1971 (2004).
25. Fernández-Marcos, M., Sanz, L., Lewis, D. R., Muday, G. K. & Lorenzo, O. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl Acad. Sci. USA 108, 18506-18511 (2011).
26. Yun, B. et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264-268 (2011).
27. Spoel, S. & Loake, G. Redox-based protein modifications: the missing link in plant immune signalling. Curr. Opin. Plant Biol. 14, 358-364 (2011).
28. Spadaro, D. et al. The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol. Plant 138, 360-371 (2010).
29. Jensen, D. E., Belka, G. K. & Du Bois, G. C. S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 331, 659-668 (1998).
30. Liu, L. et al. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494 (2001).
31. Feechan, A. et al. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl Acad. Sci. USA 102, 8054-8059 (2005).
32. Rustérucci, C., Espunya, M. C., Díaz, M., Chabannes, M. & Martínez, M. C. S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol. 143, 1282-1292 (2007).
33. Lee, U., Wie, C., Fernandez, B. O., Feelisch, M. & Vierling, E. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20, 786-802 (2008).
34. Chen, R. et al. The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res. 19, 1377-1387 (2009).
35. Frungillo, L. et al. Modulation of mitochondrial activity by S-nitrosoglutathione reductase in Arabidopsis thaliana transgenic cell lines. Biochim. Biophys. Acta 1827, 239-247 (2013).
36. Kwon, E. et al. AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236, 887-900 (2012).
37. Mur, L. A. J., Hebelstrup, K. H. & Gupta, K. J. Striking a balance: does nitrate uptake and metabolism regulate both NO generation and scavenging? Front. Plant Sci. 4, 288 (2013).
38. Streatfield, S. J. et al. The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastiddependent nuclear gene expression. Plant Cell 11, 1609-1621 (1999).
39. Planchet, E., Jagadis Gupta, K., Sonoda, M. & Kaiser, W. M. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 41, 732-743 (2005).
40. Radi, R., Cassina, A. & Hodara, R. Nitric oxide and peroxynitrite interactions with mitochondria. Biol. Chem. 383, 401-409 (2002).
41. Skelly, M. J. & Loake, G. J. Synthesis of redox-active molecules and their signaling functions during the expression of plant disease resistance. Antioxid. Redox Signal. 19, 990-997 (2013).
42. Forrester, M. T., Foster, M. W., Benhar, M. & Stamler, J. S. Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic. Biol. Med. 46, 119-126 (2009).
43. Wang, P., Du, Y., Li, Y., Ren, D. & Song, C. P. Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22, 2981-2998 (2010).
44. Seligman, K., Saviani, E. E., Oliveira, H. C., Pinto-Maglio, C. A. F. & Salgado, I. Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol. 49, 1112-1121 (2008).
45. Desikan, R., Griffiths, R., Hancock, J. & Neill, S. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acidinduced stomatal closure in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99, 16314-16318 (2002).
46. Zhao, L. et al. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134, 849-857 (2004).
47. Yamamoto-Katou, A., Katou, S., Yoshioka, H., Doke, N. & Kawakita, K. Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant Cell Physiol. 47, 726-735 (2006).
48. Moorhead, G. et al. Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin. Curr. Biol. 6, 1104-1113 (1996).
49. Su, W., Huber, S. C. & Crawford, N. M. Identification in vitro of a posttranslational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. Plant Cell 8, 519-527 (1996).
50. Kaiser, W. M. & Huber, S. C. Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J. Exp. Bot. 52, 1981-1989 (2001).
51. Foster, M. W., Forrester, M. T. & Stamler, J. S. A protein microarray-based analysis of S-nitrosylation. Proc. Natl Acad. Sci. USA 106, 18948-18953 (2009).
52. Kovacs, I. & Lindermayr, C. Nitric oxide-based protein modification: formation and site specificity of protein S-nitrosylation. Front. Plant Sci. 4, 137 (2013).
53. Gutiérrez, R. A. et al. Insights into the genomic nitrate response using genetics and the Sungear Software System. J. Exp. Bot. 58, 2359-2367 (2007).
54. Stamler, J. S., Singel, D. J. & Loscalzo, J. Biochemistry of nitric oxide and its redox-activated forms. Science 258, 1898-1902 (1992).
55. Gupta, K. J. et al. The form of nitrogen nutrition affects resistance against Pseudomonas syringae pv. phaseolicola in tobacco. J. Exp. Bot. 64, 553-568 (2013).
56. Oliveira, H. C., Justino, G. C., Sodek, L. & Salgado, I. Amino acid recovery does not prevent susceptibility to Pseudomonas syringae in nitrate reductase doubledeficient Arabidopsis thaliana plants. Plant Sci. 176, 105-111 (2009).
57. Kubienová, L. et al. Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95, 889-902 (2013).
58. Hakeem, K. R., Ahmad, A., Iqbal, M., Gucel, S. & Ozturk, M. Nitrogen-efficient rice cultivars can reduce nitrate pollution. Environ. Sci. Pollut. Res. 18, 1184-1193 (2011).
59. Guevara, D. R., El-Kereamy, A., Yaish, M. W., Mei-Bi, Y. & Rothstein, S. J. Functional characterization of rice UDP-glucose 4-epimerase 1, OsUGE1: a potential role in cell wall carbohydrate partitioning during limiting nitrogen conditions. PLoS ONE 9, e96158 (2014).
60. Murashige, T. & Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15, 473-497 (1962).
61. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629 (2006).
62. Bent, A. F. Arabidopsis in planta transformation. Uses, mechanisms, and prospects for transformation of other species. Plant Physiol. 124, 1540-1547 (2000).
63. Vitor, S. C. et al. Nitrate reductase is required for the transcriptional modulation and bactericidal activity of nitric oxide during the defense response of Arabidopsis thaliana against Pseudomonas syringae. Planta 238, 475-486 (2013).
64. Lea, U. S., Leydecker, M. T., Quilleré, I., Meyer, C. & Lillo, C. Posttranslational regulation of nitrate reductase strongly affects the levels of free amino acids and nitrate, whereas transcriptional regulation has only minor influence. Plant Physiol. 140, 1085-1094 (2006).
65. Cataldo, D. A., Haroon, M., Schrader, L. E. & Youngs, V. L. Rapid colorimetric determination of nitrate in plant tissues by nitration of salicylic acid. Commun. Soil Plant Anal. 6, 71-80 (1975).
66. Santos-Filho, P. R. et al. Nitrate reductase- and nitric oxide-dependent activation of sinapoylglucose:malate sinapoyltransferase in leaves of Arabidopsis thaliana. Plant Cell Phyiol. 53, 1607-1616 (2012).
67. Puiatti, M. & Sodek, L. Waterlogging affects nitrogen transport in the xylem of soybean. Plant Physiol. Biochem. 37, 767-773 (1999).
68. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408 (2001).
69. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W.-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17 (2005).