Nitric Oxide: A Tiny Decoder and Transmitter of Information

  • Jasmeet Kaur Abat
  • Renu Deswal


Plants are immobile, yet they are considered sentient because of their capacity to sense and respond. Priming, cross-tolerance to stress, and trans-generational traits support their capacity to retain information. Plants respond to external as well as internal cues. Signaling mechanisms are intricate, and redox changes are the hallmark of these. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) contribute to these redox changes. Nitric oxide (NO) is one such gaseous RNS which mainly modifies protein functions by post-translational modifications (PTMs) of proteins. NO is considered a “do it all” molecule. It is produced in plants by oxidative and reductive pathways. Nitrosylation, i.e., addition of NO group to thiols in proteins, is a major protein modification. Several hundreds of nitrosylated proteins and NO-modified transcription factors are identified in plants. The spatial and temporal distribution of these nitrosylated targets suggests nitrosylation to be a global modification contributing to majority of cellular functions and pathways. Some of the nitrosylated proteins are functionally validated to show these as important redox hubs in cellular physiology.

Recently, the ERF VII transcription factor-dependent N-end rule proteolysis pathway has been implicated for NO perception. A NO perceptron concept may enrich and help in integrating NO signaling in different stress conditions. Some of the redox hubs may be vital targets for crop improvement and adaptation to stress in future. Many of the nitrosylated proteins are also modified by other NO modifications like nitration or a related redox modification called glutathionylation suggesting existence of PTM crosstalk, another level of regulation which needs to be deciphered in future.


Nitric oxide Nitrosylation NO perception Abiotic stress Post-translational modification (PTM)-crosstalk NO sensor Reactive oxygen species (ROS) Glutathionylation 



The nitric oxide signaling research work was funded by the Council of Scientific and Industrial Research (CSIR), University Grants Commission (UGC), and University of Delhi, Research and Development grant.


  1. Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9:4368–4380PubMedCrossRefPubMedCentralGoogle Scholar
  2. Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata–ribulose-1, 5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J 275:2862–2872PubMedCrossRefPubMedCentralGoogle Scholar
  3. Astier J, Gross I, Durner J (2017) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411CrossRefGoogle Scholar
  4. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2013) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bellin D, Asai S, Delledonne M, Yoshioka H (2013) Nitric oxide as a mediator for defense responses. Mol Plant-Microbe Interact 26:271–277PubMedCrossRefPubMedCentralGoogle Scholar
  6. Calvo P, Sahi VP, Trewavas A (2017) Are plants sentient? Plant Cell Environ 40:2858–2869PubMedCrossRefPubMedCentralGoogle Scholar
  7. Campbell WH (1999) Nitrate reductase structure, function and regulation: bridging the gap between biochemistry and physiology. Annu Rev Plant Biol 50:277–303CrossRefGoogle Scholar
  8. Chamizo-Ampudia A, Sanz-Luque E, Llamas Á, Ocaña-Calahorro F, Mariscal V, Carreras A, Barroso JB, Galván A, Fernández E (2016) A dual system formed by the ARC and NR molybdoenzymes mediates nitrite-dependent NO production in Chlamydomonas. Plant Cell Environ 39:2097–2107PubMedCrossRefPubMedCentralGoogle Scholar
  9. Correa-Aragunde N, Foresi N, Castello FD, Lamattina L (2018) A singular nitric oxide synthase with a globin domain found in Synechococcus PCC 7335 mobilizes N from arginine to nitrate. Sci Rep 8:1–11CrossRefGoogle Scholar
  10. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. Proc Natl Acad Sci U S A 95:10328–10333PubMedPubMedCentralCrossRefGoogle Scholar
  11. Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336PubMedCrossRefGoogle Scholar
  12. Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:1–22CrossRefGoogle Scholar
  13. Furchgott RF, Cherry PD, Zawadzki JV, Jothianandan D (1984) Endothelial cells as mediators of vasodilation of arteries. J Cardiovasc Pharmacol 6:S336–S343PubMedCrossRefGoogle Scholar
  14. Gibbs DJ, Isa NM, Movahedi M, Lozano-Juste J, Mendiondo GM, Berckhan S, Marín-de la Rosa N, Conde JV, Correia CS, Pearce SP, Bassel GW (2014) Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol Cell 53:369–379PubMedPubMedCentralCrossRefGoogle Scholar
  15. Gietler M, Nykiel M, Orzechowski S, Fettke J, Zagdanska B (2016) Proteomic analysis of S-nitrosylated and S-glutathionylated proteins in wheat seedlings with different dehydration tolerances. Plant Physiol Biochem 108:507–518PubMedCrossRefGoogle Scholar
  16. Graciet E, Wellmer F (2010) The plant N-end rule pathway: structure and functions. Trends Plant Sci 15:447–453PubMedCrossRefGoogle Scholar
  17. Hu J, Huang X, Chen L, Sun X, Lu C, Zhang L, Wang Y, Zuo J (2015) Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167:1731–1746PubMedPubMedCentralCrossRefGoogle Scholar
  18. Hu J, Yang H, Mu J, Lu T, Peng J, Deng X, Kong Z, Bao S, Cao X, Zuo J (2017) Nitric oxide regulates protein methylation during stress responses in plants. Mol Cell 67:702–710PubMedCrossRefPubMedCentralGoogle Scholar
  19. Imran QM, Hussain A, Lee SU, Mun BG, Falak N, Loake GJ, Yun BW (2018) Transcriptome profile of NO-induced Arabidopsis transcription factor genes suggests their putative regulatory role in multiple biological processes. Sci Rep 8:1–14CrossRefGoogle Scholar
  20. Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GK, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci Signal 9:1–9CrossRefGoogle Scholar
  21. Kailasam S, Wang Y, Lo JC, Chang HF, Yeh KC (2018) S-Nitrosoglutathione works downstream of nitric oxide to mediate iron-deficiency signaling in Arabidopsis. Plant J 94:157–168PubMedCrossRefGoogle Scholar
  22. Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant 148:371–386PubMedCrossRefGoogle Scholar
  23. Klepper L (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ 13:537–542CrossRefGoogle Scholar
  24. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930PubMedPubMedCentralCrossRefGoogle Scholar
  25. Mayer B, Hemmens B (1997) Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem Sci 22:477–481PubMedCrossRefGoogle Scholar
  26. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125PubMedCrossRefGoogle Scholar
  27. Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I (2006) 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 171:34–40CrossRefGoogle Scholar
  28. Moncada S, Palmer RM, Higgs EA (1988) The discovery of nitric oxide as the endogenous nitrovasodilator. Hypertension 12:365–372PubMedCrossRefGoogle Scholar
  29. Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:1–17CrossRefGoogle Scholar
  30. Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103PubMedPubMedCentralCrossRefGoogle Scholar
  31. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295PubMedCrossRefPubMedCentralGoogle Scholar
  32. Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232CrossRefGoogle Scholar
  33. Sahay S, Gupta M (2017) An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67:39–52PubMedCrossRefPubMedCentralGoogle Scholar
  34. Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: Mission possible? Trends Plant Sci 21:329–340PubMedCrossRefPubMedCentralGoogle Scholar
  35. Scheres B, van der Putten WH (2017) The plant perceptron connects environment to development. Nature 543:337–345PubMedCrossRefPubMedCentralGoogle Scholar
  36. Sehrawat A, Abat JK, Deswal R (2013) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Front Plant Sci 4:1–14CrossRefGoogle Scholar
  37. Skelly MJ, Frungillo L, Spoel SH (2016) Transcriptional regulation by complex interplay between post-translational modifications. Curr Opin Plant Biol 33:126–132PubMedCrossRefPubMedCentralGoogle Scholar
  38. SoRelle R (1998) Nobel Prize awarded to scientists for nitric oxide discoveries. Circulation 98:2365–2366PubMedCrossRefPubMedCentralGoogle Scholar
  39. Spadaro D, Yun BW, Spoel SH, Chu C, Wang YQ, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Plant 138:360–371PubMedCrossRefPubMedCentralGoogle Scholar
  40. Talwar PS, Gupta R, Maurya AK, Deswal R (2012) Brassica juncea nitric oxide synthase like activity is stimulated by PKC activators and calcium suggesting modulation by PKC-like kinase. Plant Physiol Biochem 60:157–164PubMedCrossRefPubMedCentralGoogle Scholar
  41. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804PubMedCrossRefPubMedCentralGoogle Scholar
  42. Verhoeven KJ, van Gurp TP (2012) Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One 7:1–8CrossRefGoogle Scholar
  43. Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236PubMedCrossRefPubMedCentralGoogle Scholar
  44. Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176CrossRefGoogle Scholar
  45. Weisslocker-Schaetzel M, André F, Touazi N, Foresi N, Lembrouk M, Dorlet P, Frelet-Barrand A, Lamattina L, Santolini J (2017) The NOS-like protein from the microalgae Ostreococcus tauri is a genuine and ultrafast NO-producing enzyme. Plant Sci 265:100–111PubMedCrossRefPubMedCentralGoogle Scholar
  46. Wendehenne D, Pugin A, Klessig DF, Durner J (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177–183PubMedCrossRefPubMedCentralGoogle Scholar
  47. Wolters H, Jurgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317PubMedCrossRefPubMedCentralGoogle Scholar
  48. Yang L, Ji J, Wang H, Harris-Shultz KR, Abd_Allah EF, Luo Y, Guan Y, Hu X (2016) Carbon monoxide interacts with auxin and nitric oxide to cope with iron deficiency in Arabidopsis. Front Plant Sci 7:1–15Google Scholar
  49. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Jasmeet Kaur Abat
    • 1
    • 2
  • Renu Deswal
    • 2
  1. 1.Department of Botany, Gargi CollegeUniversity of DelhiNew DelhiIndia
  2. 2.Molecular Plant Physiology and Proteomics Laboratory, Department of BotanyUniversity of DelhiDelhiIndia

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