Skip to main content

Functions of NO and H2S Signal Molecules Against Plant Abiotic Stress

  • Protocol
  • First Online:
Plant Abiotic Stress Signaling

Abstract

Nitric oxide (NO) and hydrogen sulfide (H2S) are two recognized signal molecules in higher plants involved in a wide range of physiological processes and the mechanisms of response against adverse environmental conditions. These molecules can interact to provide an adequate response to palliate the negative impact exerted by stressful conditions, particularly by regulating key components of the metabolism of reactive oxygen species (ROS) to avoid their overproduction and further oxidative damage which, finally, affects cellular functioning. NO and H2S can exert the regulation over the function of susceptible proteins by posttranslational modifications (PTMs) including nitration, S-nitrosation, and persulfidation but also through the regulation of gene expression by the induction of specific transcription factors which modulate the expression of genes encoding proteins related to stress resistance. This chapter encompasses a wide perspective of the signaling and functional relationships between NO and H2S to modulate the overproduction of reactive oxygen species, particularly under abiotic stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  Google Scholar 

  2. Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Corpas FJ, Gupta DK, Palma JM (2015) Production sites of reactive oxygen species (ROS) in organelles from plant cells. In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer International Publishing, Cham

    Google Scholar 

  4. Considine MJ, Foyer CH (2021) Oxygen and reactive oxygen species-dependent regulation of plant growth and development. Plant Physiol 186(1):79–92

    Article  CAS  PubMed  Google Scholar 

  5. Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468(1):89–92

    Article  CAS  PubMed  Google Scholar 

  6. Mohn MA, Thaqi B, Fischer-Schrader K (2019) Isoform-specific NO synthesis by Arabidopsis thaliana nitrate reductase. Plants (Basel) 8:67

    Google Scholar 

  7. Corpas FJ, González-Gordo S, Palma JM (2022) NO source in higher plants: present and future of an unresolved question. Trends Plant Sci 27(2):116–119

    Article  CAS  PubMed  Google Scholar 

  8. Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199(3):633–635

    Article  CAS  PubMed  Google Scholar 

  9. Filipovic MR, Zivanovic J, Alvarez B, Banerjee R (2018) Chemical biology of H2S signaling through persulfidation. Chem Rev 118(3):1253–1337

    Article  CAS  PubMed  Google Scholar 

  10. Mukherjee S, Corpas FJ (2020) Crosstalk among hydrogen sulfide (H2S), nitric oxide (NO) and carbon monoxide (CO) in root-system development and its rhizosphere interactions: a gaseous interactome. Plant Physiol Biochem 155:800–814

    Article  CAS  PubMed  Google Scholar 

  11. Aroca A, Zhang J, Xie Y, Romero LC, Gotor C (2021) Hydrogen sulfide signaling in plant adaptations to adverse conditions: molecular mechanisms. J Exp Bot 72(16):5893–5904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mishra V, Singh VP (2021) Implication of nitric oxide and hydrogen sulfide signalling in alleviating arsenate stress in rice seedlings. Environ Pollut 291:117958

    Article  CAS  PubMed  Google Scholar 

  13. Corpas FJ, González-Gordo S, Rodriguez-Ruiz M, Muñoz-Vargas MA, Palma JM (2022) Nitric oxide and hydrogen sulfide share regulatory functions in higher plant events. Biocell 46(1):1–5

    Article  CAS  Google Scholar 

  14. González-Gordo S, Palma JM, Corpas FJ (2020) Appraisal of H2S metabolism in Arabidopsis thaliana: in silico analysis at the subcellular level. Plant Physiol Biochem 155:579–588

    Article  PubMed  Google Scholar 

  15. Campolo N, Issoglio FM, Estrin DA, Bartesaghi S, Radi R (2020) 3-Nitrotyrosine and related derivatives in proteins: precursors, radical intermediates and impact in function. Essays Biochem 64(1):111–133

    Article  CAS  PubMed  Google Scholar 

  16. Corpas FJ, González-Gordo S, Palma JM (2021) Protein nitration: a connecting bridge between nitric oxide (NO) and plant stress. Plant Stress 2:100026

    Article  CAS  Google Scholar 

  17. Muñoz-Vargas MA, González-Gordo S, Palma JM, Corpas FJ (2020) Inhibition of NADP-malic enzyme activity by H2 S and NO in sweet pepper (Capsicum annuum L.) fruits. Physiol Plant 168(2):278–288

    PubMed  Google Scholar 

  18. Corpas FJ, González-Gordo S, Cañas A, Palma JM (2019) Nitric oxide and hydrogen sulfide in plants: which comes first? J Exp Bot 70(17):4391–4404

    Article  CAS  PubMed  Google Scholar 

  19. Corpas FJ, González-Gordo S, Rodríguez-Ruiz M, Muñoz-Vargas MA, Palma JM (2022) Thiol-based oxidative posttranslational modifications (OxiPTMs) of plant proteins. Plant Cell Physiol 63(7):889–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Alvarez C, Lozano-Juste J, Romero LC, García I, Gotor C, León J (2011) Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration. J Biol Chem 286(1):578–586

    Article  CAS  PubMed  Google Scholar 

  21. Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64(4):1121–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Castillo MC, Lozano-Juste J, González-Guzmán M, Rodriguez L, Rodriguez PL, León J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8(392):ra89

    Article  PubMed  Google Scholar 

  23. Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116(4):637–647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zuccarelli R, Rodríguez-Ruiz M, Lopes-Oliveira PJ, Pascoal GB, Andrade SCS, Furlan CM, Purgatto E, Palma JM, Corpas FJ, Rossi M, Freschi L (2021) Multifaceted roles of nitric oxide in tomato fruit ripening: NO-induced metabolic rewiring and consequences for fruit quality traits. J Exp Bot 72(3):941–958

    Article  CAS  PubMed  Google Scholar 

  25. Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49(11):1711–1722

    Article  CAS  PubMed  Google Scholar 

  26. Palma JM, Mateos RM, López-Jaramillo J, Rodríguez-Ruiz M, González-Gordo S, Lechuga-Sancho AM, Corpas FJ (2020) Plant catalases as NO and H2S targets. Redox Biol 34:101525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Corpas FJ, Barroso JB, González-Gordo S, Muñoz-Vargas MA, Palma JM (2019) Hydrogen sulfide: a novel component in Arabidopsis peroxisomes which triggers catalase inhibition. J Integr Plant Biol 61(7):871–883

    CAS  PubMed  Google Scholar 

  28. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65(2):527–538

    Article  CAS  PubMed  Google Scholar 

  29. Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66(3):989–999

    Article  CAS  PubMed  Google Scholar 

  30. Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478(7368):264–268

    Article  CAS  PubMed  Google Scholar 

  31. Shen J, Zhang J, Zhou M, Zhou H, Cui B, Gotor C, Romero LC, Fu L, Yang J, Foyer CH, Pan Q, Shen W, Xie Y (2020) Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell 32(4):1000–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Muñoz-Vargas MA, González-Gordo S, Cañas A, López-Jaramillo J, Palma JM, Corpas FJ (2018) Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO. Nitric Oxide 81:36–45

    Google Scholar 

  33. Costa-Broseta Á, Castillo M, León J (2021) Post-translational modifications of nitrate reductases autoregulates nitric oxide biosynthesis in Arabidopsis. Int J Mol Sci 22(2):549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Guerra D, Ballard K, Truebridge I, Vierling E (2016) S-Nitrosation of conserved cysteines modulates activity and stability of S-nitrosoglutathione reductase (GSNOR). Biochemistry 55(17):2452–2464

    Article  CAS  PubMed  Google Scholar 

  35. Tichá T, Lochman J, Činčalová L, Luhová L, Petřivalský M (2017) Redox regulation of plant S-nitrosoglutathione reductase activity through post-translational modifications of cysteine residues. Biochem Biophys Res Commun 494(1–2):27–33

    Article  PubMed  Google Scholar 

  36. Chen S, Jia H, Wang X, Shi C, Wang X, Ma P, Wang J, Ren M, Li J (2020) Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol Plant 13(5):732–744

    Article  CAS  PubMed  Google Scholar 

  37. Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ et al (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62(13):4481–4493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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(18):4368–4380

    Article  CAS  PubMed  Google Scholar 

  39. Zhou M, Zhang J, Shen J, Zhou H, Zhao D, Gotor C, Romero LC, Fu L, Li Z, Yang J, Shen W, Yuan X, Xie Y (2021) Hydrogen sulfide-linked persulfidation of ABSCISIC INSENSITIVE 4 controls Arabidopsis ABA responses through the transactivation of mitogen-activated protein kinase kinase kinase 18. Mol Plant 14(6):921–936

    Article  CAS  PubMed  Google Scholar 

  40. He K, Guo AY, Gao G, Zhu QH, Liu XC, Zhang H, Chen X, Gu X, Luo J (2010) Computational identification of plant transcription factors and the construction of the PlantTFDB database. Methods Mol Biol 674:351–368

    Article  CAS  PubMed  Google Scholar 

  41. Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes (Basel) 10(10):771

    Article  CAS  PubMed  Google Scholar 

  42. Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126

    Article  PubMed  PubMed Central  Google Scholar 

  43. Mata-Pérez C, Sánchez-Calvo B, Padilla MN, Begara-Morales JC, Luque F, Melguizo M, Jiménez-Ruiz J, Fierro-Risco J, Peñas-Sanjuán A, Valderrama R, Corpas FJ, Barroso JB (2016) Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol 170(2):686–701

    Article  PubMed  Google Scholar 

  44. Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55(6):1080–1095

    Article  CAS  PubMed  Google Scholar 

  45. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283:9269–9275

    Google Scholar 

  46. Ahammed GJ, Li X, Mao Q, Wan H, Zhou G, Cheng Y (2021) The SlWRKY81 transcription factor inhibits stomatal closure by attenuating nitric oxide accumulation in the guard cells of tomato under drought. Physiol Plant 172(2):885–895

    Google Scholar 

  47. Wu X, Du A, Zhang S, Wang W, Liang J, Peng F, Xiao Y (2021) Regulation of growth in peach roots by exogenous hydrogen sulfide based on RNA-Seq. Plant Physiol Biochem 159:179–192

    Article  CAS  PubMed  Google Scholar 

  48. Wang Z, Dane F (2013) NAC (NAM/ATAF/CUC) transcription factors in different stresses and their signaling pathway. Acta Physiol Plant 35:1397–1408

    Article  CAS  Google Scholar 

  49. Sun Y, Song K, Guo M, Wu H, Ji X, Hou L, Liu X, Lu S (2022) A NAC transcription factor from “Sea Rice 86” enhances salt tolerance by promoting hydrogen sulfide production in rice seedlings. Int J Mol Sci 23(12):6435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhou M, Zhang J, Zhou H, Zhao D, Duan T, Wang S, Yuan X, Xie Y (2022) Hydrogen sulfide-linked persulfidation maintains protein stability of ABSCISIC ACID-INSENSITIVE 4 and delays seed germination. Int J Mol Sci 23(3):1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  52. Maruta T, Ishikawa T (2018) Ascorbate peroxidase functions in higher plants: the control of the balance between oxidative damage and signaling. In: Gupta DK, Palma JM, Corpas FJ (eds) Antioxidants and antioxidant enzymes in higher plants. Springer International Publishing, Cham

    Google Scholar 

  53. Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Aroca Á, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rodríguez-Ruiz M, Mateos RM, Codesido V, Corpas FJ, Palma JM (2017) Characterization of the galactono-1,4-lactone dehydrogenase from pepper fruits and its modulation in the ascorbate biosynthesis. Role of nitric oxide. Redox Biol 12:171–181

    Article  PubMed  PubMed Central  Google Scholar 

  56. Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555

    Article  CAS  PubMed  Google Scholar 

  57. Ma D, Ding H, Wang C, Qin H, Han Q, Hou J, Lu H, Xie Y, Guo T (2016) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS One 11:e0163082

    Article  PubMed  PubMed Central  Google Scholar 

  58. da Silva CJ, Batista Fontes EP, Modolo LV (2017) Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana. Plant Sci 256:148–159

    Article  PubMed  Google Scholar 

  59. Liu Y, Yuan Y, Jiang Z, Jin S (2022) Nitric oxide improves salt tolerance of Cyclocarya paliurus by regulating endogenous glutathione level and antioxidant capacity. Plants (Basel) 11(9):1157

    Article  CAS  PubMed  Google Scholar 

  60. Chen P, Yang W, MinxueWen, Jin S, Liu Y (2021) Hydrogen sulfide alleviates salinity stress in Cyclocarya paliurus by maintaining chlorophyll fluorescence and regulating nitric oxide level and antioxidant capacity. Plant Physiol Biochem 167:738–747

    Article  CAS  PubMed  Google Scholar 

  61. Mostofa MG, Saegusa D, Fujita M, Tran LS (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:1055

    Article  PubMed  PubMed Central  Google Scholar 

  62. Da-Silva CJ, Rodrigues AC, Modolo LV (2021) Hydrogen sulfide signaling in the defense response of plants to abiotic stresses. In: Khan MN, Siddiqui MH, Alamri S, Corpas FJ (eds) Hydrogen sulfide and plant acclimation to abiotic stresses. Springer International Publishing, Cham

    Google Scholar 

  63. Alamria SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Mohamed H, Ali HM, Alakeel KA (2019) Nitric oxide-mediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ Exp Bot 161:290–302

    Article  Google Scholar 

  64. Iqbal N, Umar S, Khan NA, Corpas FJ (2021) Nitric oxide and hydrogen sulfide coordinately reduce glucose sensitivity and decrease oxidative stress via ascorbate-glutathione cycle in heat-stressed wheat (Triticum aestivum L.) plants. Antioxidants (Basel) 10(1):108

    Article  CAS  PubMed  Google Scholar 

  65. Kharbech O, Houmani H, Chaoui A, Corpas FJ (2017) Alleviation of Cr(VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPH-recycling metabolisms. J Plant Physiol 219:71–80

    Article  CAS  PubMed  Google Scholar 

  66. Kharbech O, Sakouhi L, Ben Massoud M, Jose Mur LA, Corpas FJ, Djebali W, Chaoui A (2020) Nitric oxide and hydrogen sulfide protect plasma membrane integrity and mitigate chromium-induced. Plant Physiol Biochem 157:244–255

    Article  CAS  PubMed  Google Scholar 

  67. Zhang H, Hu LY, Li P, Hu KD, Jiang CX, Luo JP (2010) Hydrogen sulfide alleviated chromium toxicity in wheat. Biol Plant 54:743–747

    Article  CAS  Google Scholar 

  68. Kaya C, Ashraf M, Alyemeni MN, Corpas FJ, Ahma P (2020) Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by upregulating the ascorbate-glutathione cycle and glyoxalase system. J Hazard Mater 398:122882

    Google Scholar 

  69. Mishra V, Singh P, Tripathi DK, Corpas FJ, Singh VP (2021) Nitric oxide and hydrogen sulfide: an indispensable combination for plant functioning. Trends Plant Sci 26(12):1270–1285

    Google Scholar 

  70. Seabra AB, Silveira NM, Ribeiro RV, Pieretti JC, Barroso JB, Corpas FJ, Palma JM, Hancock JT, Petřivalský M, Gupta KJ, Wendehenne D, Loake GJ, Durner J, Lindermayr C, Molnár Á, Kolbert Z, Oliveira HC (2022) Nitric oxide-releasing nanomaterials: from basic research to potential biotechnological applications in agriculture. New Phytol 234(4):1119–1125

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Francisco J. Corpas and José M. Palma research is supported by European Regional Development Fund-cofinanced grants from the Spanish Ministry of Science and Innovation (PID2019-103924GB-I00), and the Plan Andaluz de Investigación, Desarrollo e Innovación (P18-FR-1359), Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco J. Corpas .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Corpas, F.J., Palma, J.M. (2023). Functions of NO and H2S Signal Molecules Against Plant Abiotic Stress. In: Couée, I. (eds) Plant Abiotic Stress Signaling. Methods in Molecular Biology, vol 2642. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3044-0_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-3044-0_5

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-3043-3

  • Online ISBN: 978-1-0716-3044-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics